Ecology Genetic Considerations in Plant Ecological Restoration
by
Danny J. Gustafson, Alexis Gibson
  • LAST REVIEWED: 06 May 2016
  • LAST MODIFIED: 30 October 2019
  • DOI: 10.1093/obo/9780199830060-0076

Introduction

Ecological restoration is most commonly described as the process of aiding in the recovery of a damaged or destroyed system. In many cases, restoration may not be possible when self-sustaining populations, functions, and trajectories cannot be maintained due to the type of disturbance sustained by a site; in these cases, revegetation or remediation are more achievable goals. The definition of ecological restoration has been expanded to incorporate scientific inquiry into the process of the recovery of a natural range of ecosystem composition, structure, and dynamics. Ecological restoration research spans different levels of organization from genes to ecosystems. Genetic considerations are fundamental to the success of ecological restoration, and considerations of this issue will impact choices from seed source selection to genetic control of ecosystem services. A major decision for restorationists is the use of local versus nonlocal plant material, as well as the mixing of source populations; ideally, these choices can be based on sound population genetic, ecological, and evolutionary theory research. Ultimately, selection of plant material to be used in ecological restoration is driven by the specific project goals, availability and quality of plant materials, site conditions, and scale of the project. Beyond the local versus nonlocal selection issue, genetic issues related to small population dynamics, gene flow in the modern landscape, and gene expression affecting community structure and ecosystem functions can affect the success of ecological restoration activities. This article focuses primarily on plants; however, issues related to genetics of small populations (inbreeding and outbreeding depression, founder effects, and fitness consequences of reduced genetic variation) are important considerations for animal species too. The readings contained within this bibliography include: Ecotypic Variation, Seed Provenance for Restoration, Seed Transfer Zones for Restoration, Seed Provenance for Revegetation, Life History Traits, Moving beyond Neutral Markers, Inbreeding Depression, Outbreeding Depression, Founder Effects, Fitness Consequences of Reduced Genetic Variation, Community and Landscape Genetics, Testing Genotypic Effects on Community and Ecosystem Processes, Evaluating Success, and Genetic Composition and Diversity in Restored Populations.

General Overviews

Genetic considerations for plant ecological restoration link individual genotypic performance to ecosystem function. For those interested in this topic, numerous general resources provide a foundation for understanding how genetic considerations interact with plant materials selection. Foundations of Ecological Restoration (Falk, et al. 2006), published by Island Press in cooperation with the Society for Ecological Restoration International (SER), provides sixteen chapters written by international experts and is organized into three broad sections (ecological theory and the restoration of populations and communities, restoring ecological function, and restoration ecology in context). Included in this essential text is a chapter on population and ecological genetics in restoration ecology that is an updated and expanded version of an earlier introduction to restoration genetics, Falk, et al. 2001. A second edition, Palmer, et al. 2016 updates and expands the advances in the field of restoration ecology. Introduction to Conservation Genetics (Frankham, et al. 2010) provides a sound foundation in population genetics with real-world case studies. In addition, Introduction to Conservation Genetics (Frankham, et al. 2010) provides a thorough foundation in population genetic with real-world case studies. The seminal work of Falk and Holsinger 1991 articulates population biology and genetics concerns for small plant populations as well as provides strategies for sampling and conservation genetic variation. Bowles and Whelan 1994 includes chapters on genetic considerations, life-history traits, and species interactions when restoring endangered plant and animal species. While the case studies are primarily from the Great Plains and western North America, Rogers and Montalvo 2004 considers genetic diversity and genetic integrity essential components of source material selection for restoration using native plant species. Guerrant, et al. 2004 demonstrates the value of ex situ facilities (i.e., botanical gardens and seed banks) to species conservation and restoration. Of particular interest to genetic considerations for ecological restoration are the two chapters on population genetic issues and quantitative genetics. The Center for Plant Conservation is a network of fifty-seven leading botanical institutions whose primary mission is to conserve and restore imperiled native plants of the United States. This organization coordinates a national ex situ rare plant material conservation program that ensures that material is available for restoration and recovery efforts, technical assistance, and educational and advocacy support through the network, national office, and online resources. Although focused on rare plant species, Maschinski and Albrecht 2017 provides a succinct overview from the Center for Plant Conservation of best practice guidelines for reintroduction that are applicable for any plant restoration project.

  • Bowles, Marlin L., and Christopher J. Whelan, eds. 1994. Restoration of endangered species: Conceptual issues, planning and implementation. New York: Cambridge Univ. Press.

    DOI: 10.1017/CBO9780511623325Save Citation »Export Citation »E-mail Citation »

    A collection and expansion of papers from a Symposium on Recovery and Restoration of Endangered Plants and Animals organized for the Second Annual Conference of the Society for Ecological Restoration held in Chicago, Illinois, 1990. This book includes influential chapters on plant population genetics (Fenster and Dudash), reproductive biology and life history traits (Weller), and plant-insect interactions (Louda).

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    • Center for Plant Conservation.

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      The Center for Plant Conservation (CPC) online resource provides links to fifty-seven leading partner botanical institutions, searchable taxon links, a conservation directory, and resources. “Plant Links” provides access to online databases, organizations (state to international), native plant societies, and natural heritage programs. “Conservation Directory” is searchable by state, expertise, and name.

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      • Falk, Donald A., and Kent E. Holsinger, eds. 1991. Genetics and conservation of rare plants. Oxford: Oxford Univ. Press.

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        Seminal work in plant conservation genetics because of its thoughtful coverage of a wide range of issues related to rare plant biology and conservation. The book, which, according to its preface, grew from papers originally presented at a Conference on the Genetics and Conservation of Rare Plants coordinated by the Center for Plant Conservation and held at the Missouri Botanical Garden in St. Louis in March 1989, is organized into five sections, is well written, and very approachable for graduate students as well as professional scientists.

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        • Falk, Donald A., Eric E. Knapp, and Edgar O. Guerrant. 2001. An introduction to restoration genetics. Washington, DC: Society for Ecological Restoration.

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          Useful for practitioners with limited population genetics training, discusses authenticity (accuracy) restoration versus restoring a functional population/community, complexities of source material selection (space for genotype substitution, 1,000-foot elevation bands or 100 miles lateral distance), and offers a helpful section on sampling the diversity of source populations.

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          • Falk, Donald A., Margaret A. Palmer, and Joy B. Zedler, eds. 2006. Foundations of restoration ecology. Washington, DC: Island Press.

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            Essential resource for ecological restoration researchers and practitioners. Chapter 5, “Population and Ecological Genetics in Restoration Ecology” (pp. 123–152), provides a succinct and well-written review of genetic considerations for restoring plant populations.

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            • Frankham, Richard, Jonathan D. Ballou, and David A. Briscoe. 2010. Introduction to conservation genetics. 2d ed. Cambridge, UK: Cambridge Univ. Press.

              DOI: 10.1017/CBO9780511809002Save Citation »Export Citation »E-mail Citation »

              The book illustrates topics such as evolutionary genetics, loss of diversity, inbreeding, population fragmentation, taxonomic uncertainties, the genetic management of threatened species, and molecular genetics with real-world examples. Reference to statistical genetic packages is helpful for early carrier restoration professionals. Written for advanced undergraduates and graduate students.

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              • Guerrant, Edward O., Kayri Havens, and Mike Mauder, eds. 2004. Ex situ plant conservation: Supporting species survival in the wild. Science and Practice of Ecological Restoration. Washington, DC: Island Press.

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                Ex situ conservation has a vital role in conservation programs throughout the world. Ethical and philosophical concerns of ex situ programs, common horticultural practices, genetic considerations for sampling, seed storage, and management of collections are addressed in this edited book.

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                • Maschinski, Joyce, and Matthew A. Albrecht. 2017. Center for Plant Conservations’s best practice guidelines for the reintroduction of rare plants. Plant Diversity 39.6: 390–395.

                  DOI: 10.1016/j.pld.2017.09.006Save Citation »Export Citation »E-mail Citation »

                  Short review of the best management practices for plant reintroductions, advocating for genetic considerations based on empirical data, developing a meaningful monitoring, and conducting reintroductions as experiments.

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                  • Palmer, Margaret A., Joy B. Zedler, and Donald A. Falk, eds. 2016. Foundations of restoration ecology. 2d ed. Washington, DC: Island Press.

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                    This second edition incorporates advanced work in the field of restoration ecology, expands the scope of the topics covered, and provides examples of how theory informs on-the-ground restoration efforts.

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                    • Rogers, Deborah L., and Arlee M. Montalvo. 2004. Genetically appropriate choices for plant materials to maintain biological diversity. Report to the USDA Forest Service, Rocky Mountain Region. Lakewood, CO: Univ. of California.

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                      This extensively referenced document is organized from genetic principles to specific decisions to case studies. The first several chapters address why genetic diversity and genetic integrity are important to native plant species, the relationship between genetics and ecology, and genetic selection of plant materials followed by case studies. The authors also provide a process for aiding decisions about seed sourcing.

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                      Journals

                      Hundreds of journals publish articles relevant to genetic issues in ecological restoration. The top-ranked ecology and evolution journals include Ecology, Journal of Ecology, Evolution, Molecular Ecology, and Trends in Ecology & Evolution. A number of disciplines, including conservation, as well as the Society for Ecological Restoration International have specialist journals that publish articles on conservation genetics and restoration genetics that are extremely valuable sources for restoration genetic issues. Conservation Biology and Biological Conservation are the top journals in conservation. In restoration ecology, the premier journal is Restoration Ecology. General plant biology journals, such as American Journal of Botany, publish articles on pollination, life history traits, population biology, phylogeography, and reproduction biology that are also valuable for integrating the biology, ecology, and genetics in species reintroductions.

                      Ecotypic Variation

                      Classic reciprocal transplant studies conducted by the author of Turesson 1922 established the connection between local environmental conditions and plant adaptations, which Turesson has termed ecotypes. Clausen and Hiesey 1958 provides an example of landscape-level population variation by showing genetic control of ecotypic variation in several North American species based on elevation/environmental gradients. In the expansive Great Plains of North America, McMillan 1959 further demonstrates ecotypic variation in perennial native grasses driven by precipitation and temperature gradients across large geographic areas. These studies provide the foundation for our understanding of how local environmental conditions can select for the most-fit locally adapted ecotype, which has significant ramifications for plant materials selection in ecological restoration. Linhart and Grant 1996 provides one of the first reviews of natural biotic and abiotic selection driving plant population differentiation across multiple spatial scales. Kawecki and Ebert 2004 provides a conceptual review of evolutionary theory as it relates to local adaption, while Hufford and Mazer 2003 specifically reviews genetic issues of plant ecotypic variation as they relate to ecological restoration in the modern landscape. A meta-analysis of local adaptation in plants, Leimu and Fisher 2008 shows local plants tended to outperform nonlocal plants, while the degree of adaptation was independent of life-history traits, geographic distance, or habitat, and local adaptation was rare in small populations (<1,000 flowering individuals). A review of plant, animal, fungi, and protist studies, Hereford 2009 shows higher local composite fitness (fecundity and viability) when environmental differences were greater between the reciprocal transplant sites. While numerous studies have shown ecotypic variation in native plant populations, Gibson, et al. 2016 shows that very few of these studies have been conducted under conditions similar to those seen in restoration projects. A challenge in determining whether populations show ecotypic variation can be that patterns of adaptive variation in traits may take years or decades to appear (Germino, et al. 2019). The ecotypic variation field studies and literature reviews provide the scientific basis for selecting local genotypes for local restorations; however, rarely are there locally adapted, genetically diverse donor populations within close proximity to the proposed restoration site.

                      • Clausen, Jens, and William M. Hiesey. 1958. Experimental studies on the nature of species: IV; Genetic structure of ecological races. Washington, DC: Carnegie Institution of Washington.

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                        Culmination of detailed genetics of ecotypic variation of Potentilla glandulosa, with reference to the authors’ previous extensive research in the Carnegie Institution of Washington publications 520 (1940) and 581 (1948).

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                        • Germino, Matthew J., Ann M. Moser, and Alan R. Sands. 2019. Adaptive variation, including local adaptation, requires decades to become evident in common gardens. Ecological Applications 29.2: e01842.

                          DOI: 10.1002/eap.1842Save Citation »Export Citation »E-mail Citation »

                          Populations of Artemisia tridentata ssp wyomingensis did not exhibit differences in survival between local and non-local populations until >10 years in the common garden.

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                          • Gibson, Alexis, Erin K. Espeland, Viktoria Wagner, and Cara R. Nelson. 2016. Can local adaptation research in plants inform selection of native plant materials? An analysis of experimental methodologies. Evolutionary Applications 9.10: 1219–1228.

                            DOI: 10.1111/eva.12379Save Citation »Export Citation »E-mail Citation »

                            Reviews methods of local adaptation papers to identify similarity between research conditions and restoration. The majority of studies take place over short time periods in agricultural conditions, include a limited number of selective factors, do not use population growth rate as a measure of fitness, and focus on later life stages without including germination or emergence.

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                            • Hereford, Joe. 2009. A quantitative survey of local adaptation and fitness trade-offs. American Naturalist 173.5: 579–588.

                              DOI: 10.1086/597611Save Citation »Export Citation »E-mail Citation »

                              Focuses on local adaptation and potential trade-offs in multiple environments with plant (50), animal (21), fungi (1), and protist (1) studies. Trade-offs in local adaptation were stronger when home site environmental differences were greater, and the magnitude of local adaptation was greatest when measuring composite fitness (fecundity and viability).

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                              • Hufford, Kristina M., and Susan Mazer. 2003. Plant ecotypes: Genetic differentiation in the age of ecological restoration. Trends in Ecology & Evolution 18.3: 147–155.

                                DOI: 10.1086/597611Save Citation »Export Citation »E-mail Citation »

                                Reviews genetic considerations (founder effects, genetic swamping, heterosis, outbreeding and inbreeding depression) for population conservation and restoration and highlights experimental studies documenting F1 and F2 intraspecific hybrid performance. Inclusion of intraspecific hybrid performance is important for the long-term population viability when considering seed transfer zones for restoration.

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                                • Kawecki, Tadeusz J., and Dieter Ebert. 2004. Conceptual issues in local adaptation. Ecology Letters 7.12: 1225–1241.

                                  DOI: 10.1111/j.1461-0248.2004.00684.xSave Citation »Export Citation »E-mail Citation »

                                  Well-written overview of evolutionary theory as it relates to population genetics of local adaptation. Not intended as a review of local adaptation studies, but to provide a larger context of evolution and population genetic theory for studying processes of local adaptation.

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                                  • Leimu, Roosa, and Markus Fisher. 2008. A meta-analysis of local adaptation in plants. PLoS ONE 3.12: e4010.

                                    DOI: 10.1371/journal.pone.0004010Save Citation »Export Citation »E-mail Citation »

                                    In a meta-analysis of reciprocal transplant studies, local plants typically outperformed nonlocal plants; however, only 45 percent of the population comparisons showed reciprocal local advantages. The degree of local adaption was independent of life history, geographic distance, and habitat. Local adaptation was rare in small (< 1000 flowering individuals) populations. Genetic diversity is essential for population adaptation.

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                                    • Linhart, Yan B., and Michael C. Grant. 1996. Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 24:237–277.

                                      DOI: 10.1146/annurev.ecolsys.27.1.237Save Citation »Export Citation »E-mail Citation »

                                      Genetic differentiation among plant populations over small spatial scales (cm to m) can result from a variety of biotic and abiotic factors. Natural selection at these small spatial scales drives the genetic architecture in natural plant populations.

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                                      • McMillan, Calvin. 1959. The role of ecotypic variation in the distribution of the central grassland of North America. Ecological Monographs 29.4: 285–308.

                                        DOI: 10.2307/1942132Save Citation »Export Citation »E-mail Citation »

                                        Seminal ecotypic variation research with North American grass species through common garden, observational, and experimental research.

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                                        • Turesson, Gote. 1922. The genotypical response of the plant species to the habitat. Hereditas 3:211–350.

                                          DOI: 10.1111/j.1601-5223.1922.tb02734.xSave Citation »Export Citation »E-mail Citation »

                                          Studies the influence of local environmental conditions on plant adaptations, if these adaptations provided a fitness advantage, and if these adaptations have a genetic basis driven by local environmental conditions.

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                                          Seed Provenance for Restoration

                                          Selection of local ecotypes is the gold standard for ecological restoration with the assumption that locally adapted gene complexes will provide a fitness advantage over nonlocal genotypes; however, there is often a need to source seeds from multiple populations in order to develop a large, genetically robust restored population, which complicates the definition of local. Lesica and Allendorf 1999 is one of the first papers to establish the conceptual framework for plant material selection in ecological restoration. The authors incorporated restoration site attributes in plant source selection, e.g., mixing multiple population sources for highly disturbed sites. In the must-read review “How Local Is Local?” (McKay, et al. 2005), the authors present evolutionary and population genetic theories relevant to restoration ecology. Vander Mijnsbrugge, et al. 2009, a review of genetic adaptations of North American and European woody and herbaceous species, recommends ecological matching between donor site and restoration site. These three review papers advocate similar “practical rules” of using local, if possible, basing “local” on similar ecological settings (ecological matching), and minimizing any seed selection bias during seed increase practices. Development of seed provenance guidelines should include ecological and climatic drivers of plant adaptation, according to Vogel, et al. 2005; however, biotic and abiotic factors could drive local adaptation. Bucharova, et al. 2018 suggests combining seeds from several large populations centered on a target restoration site “regional admixture provenancing” as a method to preserve locally adapted traits while creating genetically diverse restoration seed mixes. Krauss and Koch 2004 proposes spatial genetic analysis of molecular markers as a means for delineating seed provenances, which was later used to establish seed provenances for Persoonia longifolia (Stingemore and Krauss 2013). However, the use of molecular markers assumes isolation by distance patterns that reflect adaptive variation patterns. Reciprocal transplant and common garden studies have been used to assess seed provenance delineation with mixed results even with co-occurring species in the same community (Bischoff, et al. 2010; Miller, et al. 2011). Establishing seed provenance guidelines that can be used for multiple species is complicated because selection driving local adaptation may be species specific and ecological context driven.

                                          • Bischoff, Armin, Thomas Steinger, and Heinz Muller-Scharer. 2010. The importance of plant provenance and genotypic diversity of seed material used for ecological restoration. Restoration Ecology 18.3: 338–348.

                                            DOI: 10.1111/j.1526-100X.2008.00454.xSave Citation »Export Citation »E-mail Citation »

                                            Tested provenance differentiation of four common plant species used in ecological compensation wildflower strips planted in Swiss agricultural areas. The authors found differences among provenances, but no general local advantage, and productivity increased with genotypic diversity.

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                                            • Bucharova, Anna, Oliver Bossdorf, Norbert Hölzel, J Johannes Kollmann, Rüdiger Prasse, and Walter Durka. 2018. Mix and match: Regional admixture provenancing strikes a balance among different seed-sourcing strategies for ecological restoration. Conservation Genetics 20.1: 7–17.

                                              DOI: 10.1007/s10592-018-1067-6Save Citation »Export Citation »E-mail Citation »

                                              The authors present a framework for identifying climatic regions around restoration sites; this practice is called “regional admixture provenancing” and is currently used in Germany. The benefits of this practice are (1) that it allows restorationists to pre-identify climatic or environmental zones for seed collection, and (2) mixing seeds from multiple populations helps avoid genetic issues in small populations such as founder effects, inbreeding depression, or limited genetic diversity.

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                                              • Krauss, Siegfried, and John M. Koch. 2004. Rapid genetic delineation of provenance for plant community restoration. Journal of Applied Ecology 41.6: 1162–1173.

                                                DOI: 10.1111/j.0021-8901.2004.00961.xSave Citation »Export Citation »E-mail Citation »

                                                Used neutral markers (AFLP) and spatial autocorrelation to delineate seed provenances for four common species used in Australian mine revegetation. Limitations of this approach are discussed and center on experimental design and analysis issues related to small sample sizes.

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                                                • Lesica, Peter, and Fred W. Allendorf. 1999. Ecological genetics and the restoration of plant communities: Mix or match? Restoration Ecology 7.1:42–50.

                                                  DOI: 10.1046/j.1526-100X.1999.07105.xSave Citation »Export Citation »E-mail Citation »

                                                  One of the first studies to articulate a conceptual framework for plant material for community restoration and link proposed site attributes to selection. Local plants if disturbance is low, mixes of multiple populations for highly disturbed sites, and cultivated varieties may be appropriate in limited situations.

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                                                  • McKay, John K., Caroline E. Christian, Susan Harrison, and Kevin J. Rice. 2005. “How local is local?”—A review of practical and conceptual issues in the genetics of restoration. Restoration Ecology 13.3: 432–440.

                                                    DOI: 10.1111/j.1526-100X.2005.00058.xSave Citation »Export Citation »E-mail Citation »

                                                    Presents evolutionary and population genetic theory relevant to genetics of restoration in easy-to-understand language. The practical recommendations are based on years of experience and sound scientific investigation: local if possible, ecological matching, life history traits will help predict population dynamics, and minimize unintentional selection during seed increase practices.

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                                                    • Miller, Stephanie A., Amy Bartow, Melanie Gisler, Kimiora Ward, Amy S. Young, and Thomas N. Kaye. 2011. Can an ecoregion serve as a seed transfer zone? Evidence from a common garden study with five native species. Restoration Ecology 19.201: 268–276.

                                                      DOI: 10.1111/j.1526-100X.2010.00702.xSave Citation »Export Citation »E-mail Citation »

                                                      Study of morphological and phenological traits of five species used in prairie restorations. One of four species showed associations between geographic distance and plant performance within the Willamette Valley Level III Ecoregion, indicating a single seed transfer zone corresponding to the ecoregion is appropriate for three of the four species.

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                                                      • Stingemore, Jessica A., and Siegfried L. Krauss. 2013. Genetic delineation of local provenance in Persoonia longifolia: Implications for seed sourcing for ecological restoration. Restoration Ecology 21.1: 49–57.

                                                        DOI: 10.1111/j.1526-100X.2011.00861.xSave Citation »Export Citation »E-mail Citation »

                                                        Used AFLP markers, geographic, and environmental data to estimate local seed provenance for the endemic Australian tree species Persoonia longifolia.

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                                                        • Vander Mijnsbrugge, Kristine, Armin Bischoff, and Barbara Smith. 2009. A question of origin: Where and how to collect seed for ecological restoration. Basic and Applied Ecology 11.4: 300–311.

                                                          DOI: 10.1016/j.baae.2009.09.002Save Citation »Export Citation »E-mail Citation »

                                                          Considers North American and European woody and herbaceous species when reviewing genetics of adaptation, but decidedly European models of seed transfer and legislation. Seed collection and use, engage stake holders, and document activities recommendations consistent with similar “practical rule” papers.

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                                                          • Vogel, K. P., M. R. Schmer, and R. B. Mitchell. 2005. Plant adaptation regions: Ecological and climatic classification of plant materials. Rangeland Ecology and Management 58:315–319.

                                                            DOI: 10.2111/1551-5028(2005)58[315:PAREAC]2.0.CO;2Save Citation »Export Citation »E-mail Citation »

                                                            The authors merged the ecoregion and plant hardiness zone maps to form the 145 Plant Adaptation Regions (PARs) for the United States. PARs provide an ecological and climatic structure for selecting sites to evaluate plant materials, but the system does not address biotic and abiotic factors that may drive local adaptations.

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                                                            Seed Transfer Zones for Restoration

                                                            In areas where a large amount of native seed is required for restoration activities, seed transfer zones can give managers landscape-specific boundaries delineating which populations can be combined without losing beneficial traits and where the resulting seed mixes can be used. In the early 20th century, foresters began developing seed transfer zones to increase success in planting commercially important trees; the goal of seed transfer zones is to develop geographic boundaries for a region and species of interest based on traits assessed under common garden conditions. Johnson, et al. 2004 provides general guidance on this history and how these same methods can be applied to create seed transfer zone boundaries for non-tree species, while St. Clair, et al. 2013 is one example of developing species-specific seed transfer zones. Compared to seed provenancing strategies such as watershed boundaries or areas of general ecological similarity, seed transfer zones are based on empirical relationships between potentially adaptive traits and abiotic (primarily climatic) selective factors. This allows managers to collect seeds from a large number of populations and then either store or agriculturally increase seeds for use in large-scale or unexpected restoration conditions. However, species-specific transfer zones can be time consuming and expensive to develop. Researchers have tried to identify alternative methods for constructing zones ranging from Bower, et al. 2014 generalized climatic zones that do not rely on species-specific data to Doherty, et al. 2017, which identifies areas where source seeds could be used based on climatic similarity. Expanding on the method of developing species-specific transfer zones without a common garden, Crow, et al. 2018 discusses using species distribution models and environmental tolerance to create species-specific transfer models without using a common garden. In many cases, generalized regions for seed transfer show suitability for restoration seed movement. Gustafson, et al. 2018 documents significant genetic structure among seed transfer zones of two perennial dominant longleaf pine understory species of the North American coastal plains. These seed transfer zones were based on terrestrial ecoregions, further subdivided by major river drainages, and empirically tested in a six species, multiple common garden study (Giencke, et al. 2018). Durka, et al. 2017 finds that seven grassland species in Germany showed genetic clustering consistent with genetic differences among pre-defined German seed transfer zones. Gibson, et al. 2019 shows that transfer zone boundaries may be improved by including other selective factors that act at the landscape scale, such as soils.

                                                            • Bower, Andy D., J. Bradley St. Clair, and Vicky Erickson. 2014. Generalized provisional seed zones for native plants. Ecological Applications 24.5: 913–919.

                                                              DOI: 10.1890/13-0285.1Save Citation »Export Citation »E-mail Citation »

                                                              The authors develop climate-based general seed transfer zones for the United States by combining an aridity metric and winter minimum temperatures bands, resulting in provisional seed zones for the continental United States.

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                                                              • Crow, Taylor M., Shannon E. Albeke, C. Alex Buerkle, and Kristina M. Hufford. 2018. Provisional methods to guide species-specific seed transfer in ecological restoration. Ecosphere 9.1: e02059.

                                                                DOI: 10.1002/ecs2.2059Save Citation »Export Citation »E-mail Citation »

                                                                Presents an alternative method for constructing seed transfer zone boundaries using species distribution models and multivariate statistics for the native Cercocarpus montanus. Performance of transfer zone models generated using this method is compared to other potential generalized seed transfer zone options, including ecoregions.

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                                                                • Doherty, Kyle D., Bradley J. Butterfield, and Troy E. Wood. 2017. Matching seed to site by climate similarity: Techniques to prioritize plant materials development and use in restoration. Ecological Applications 27.3: 1010–1023.

                                                                  DOI: 10.1002/eap.1505Save Citation »Export Citation »E-mail Citation »

                                                                  The authors present a method to identify areas where existing seed sources could be used based on a climatic similarity index between the source and a given area on the landscape. In situations where seed transfer zones are not practical or cost-effective to develop, this method can be useful for managers in determining where an existing seed source could be used or in identifying areas to target future seed collections.

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                                                                  • Durka, Walter, Stefan G, Michalski, Kenneth W. Berendzen, et al. 2017. Genetic differentiation within multiple common grassland plants supports seed transfer zones for ecological restoration. Journal of Applied Ecology 54.1: 116–126.

                                                                    DOI: 10.1111/1365-2664.12636Save Citation »Export Citation »E-mail Citation »

                                                                    Authors analyzed genetic structure in seven common German grassland plant species to determine genetic population structure. All species showed genetic clustering consistent with the eight preexisting seed transfer zone boundaries, indicating that the transfer zones capture a majority of genetic variation.

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                                                                    • Gibson, Alexis, Cara R. Nelson, Susan Rinehart, Vince Archer, and Aram Eramian. 2019. Importance of considering soils in seed transfer zone development: Evidence from a study of the native Bromus marginatus. Ecological Applications 29.2: e.01835.

                                                                      DOI: 10.1002/eap.1835Save Citation »Export Citation »E-mail Citation »

                                                                      Seed transfer zones are generally developed using widespread climatic data; the authors in this paper find that for Bromus marginatus, including soils variables increased the trait variation explained by transfer zone models.

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                                                                      • Giencke, Lisa M., R. Carol Denhof, L. Katherine Kirkman, O. Stribling Stuber, and Steven T. Brantley. 2018. Seed sourcing for longleaf pine ground cover restoration: Using plant performance to assess seed transfer zones and home-site advantage. Restoration Ecology 26.6: 1127–1136.

                                                                        DOI: 10.1111/rec.12673Save Citation »Export Citation »E-mail Citation »

                                                                        Authors empirically tested a suite of provisional seed transfer zones at multiple geographic scales with six dominant perennial herbaceous species of the longleaf pine ecosystem in a reciprocal transplant, multiple common garden study. Seed transfer zones were a good predictor of plant performance and provide landscape level guidance for native plant material producers and natural resource managers.

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                                                                        • Gustafson, Danny J., Karen Harris-Shultz, Parker E. Gustafson, Lisa M. Giencke, R. Carol Denhof, and L. Katherine Kirkman. 2018. Seed sourcing for longleaf pine herbaceous understory restoration: Little bluestem (Schizachyrium scoparium) and hairy lespedeza (Lespedeza hirta). Natural Areas Journal 38.5: 380–392.

                                                                          DOI: 10.3375/043.038.0507Save Citation »Export Citation »E-mail Citation »

                                                                          Restoration genetic study of two dominant understory perennial species of the longleaf pine ecosystem. These coastal plains seed transfer zones follow the Nature Conservancy terrestrial ecoregions with the extensive East Gulf Coastal Plain subdivided by major river drainages. Coastal plains transfer zone plant material were genetically different from non-coastal plains commercial sources, there was significant genetic structure among transfer zones, and transfer zone genetic relationships roughly follow geographic proximity.

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                                                                          • Johnson, G. R., Frank C. Sorensen, John Bradley St Clair, and Richard C. Cronn. 2004. Pacific Northwest forest tree seed zones: a template for native plants? Native Plants 5:131–140.

                                                                            DOI: 10.2979/NPJ.2004.5.2.131Save Citation »Export Citation »E-mail Citation »

                                                                            A discussion of the history of seed transfer zones (especially in the Pacific Northwest of the United States) and the rational for how transfer zones are constructed.

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                                                                            • St. Clair, John Bradley, Francis F. Kilkenny, Richard C. Johnson, Nancy L. Shaw, and George Weaver. 2013. Genetic variation in adaptive traits and seed transfer zones for Pseudoroegneria spicata (bluebunch wheatgrass) in the northwestern United States. Evolutionary Applications 6.6: 933–948.

                                                                              DOI: 10.1111/eva.12077Save Citation »Export Citation »E-mail Citation »

                                                                              The authors develop a climate-based seed transfer zone map for the common grass Pseudoroegnaria spicata in the western United States based on data collected in several common gardens. The authors use methods similar to those used in other seed transfer zone studies in grasses, shrubs, and forbs, and the paper serves as a good starting point for those interested in developing this type of transfer zone map.

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                                                                              • US Forest Service. TRM Seed Zone Applications.

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                                                                                A valuable website collecting all of the current seed transfer zones resulting from US Forest Service research. Resources include an interactive map showing the suggested generalized or species-specific seed transfer zone for a given location in the United States, peer-reviewed publications underlying the development of the transfer zones, and downloadable shapefiles and maps.

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                                                                                Seed Provenance for Revegetation

                                                                                Revegetation and reclamation projects tend to be associated with large areas of habitat where reestablishment of the historical plant community may not be possible due to a history of severe disturbance. Restoration of ecosystem services is consistent with the mission of ecological restoration; however, revegetation and reclamation projects are considered different from restoring functional historical plant communities in this article. Jones 2003 proposes a Restoration Gene Pool (RGP) organizational scheme based on plant material (local seeds, multiple origin polycrosses, improved cultivars, and noninvasive species) and site conditions (disturbance history). Focusing on the best seed sources for restoration of ecosystem services on large highly disturbed habitats, Johnson, et al. 2010 advocates for use of regionally appropriate plant material with sufficient genetic variation to provide the restored populations the best chance to establish and evolve. This is very different from the historical plant breeder directional selection/crop improvement programs of the past. Broadhurst, et al. 2010 and Breed, et al. 2013 advocate increasing the genetic diversity in seed mixes, which is essential for populations to adapt to changing environmental conditions, especially when considering habitat fragmentation and climate change. Havens, et al. 2015 suggests collecting seed during difficult years or sites as a way to increase the chance plant populations can adapt to difficult conditions predicted under climate change. Harris, et al. 2006 promotes restoring ecosystem services rather than matching plant communities in reference systems because current and future environmental conditions may not support historical reference plant communities. Koskela, et al. 2013 endorses establishing minimum viable population criteria based on additive genetic variation rather than allelic variance for genetic management of pan-European forest tree genetic diversity. Assessing the genetic risk of seed sources in revegetation should balance the potential benefits of restoring ecosystem function with potential negative effects on surrounding natural plant communities (Weeks, et al. 2011). Governmental agencies, such as the US Forest Service, may provide a wealth of online resources addressing issues from native plant material selection; seed testing and nursery practices; and low-tech solutions to collecting, processing, and planting seeds to genetic risks of plant material selection (US Forest Service).

                                                                                • Breed, Martin F., Michael G. Stead, Kym M. Ottewell, Michael G. Gardner, and Andrew J. Lowe. 2013. Which provenance and where? Seed sourcing strategies for revegetation in a changing environment. Conservation Genetics 14.1: 1–10.

                                                                                  DOI: 10.1007/s10592-012-0425-zSave Citation »Export Citation »E-mail Citation »

                                                                                  Focus on revegetation rather than restoration, but incorporates climate change and habitat fragmentation in the review of four strategies for selecting provenances. Promotes evidence-based strategies and long-term experiments to better inform seed provenance guidelines.

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                                                                                  • Broadhurst, Linda M., Andrew Lowe, David Coates, et al. 2010. Seed supply for broadscale restoration: Maximizing evolutionary potential. Ecological Applications 1.4: 587–597.

                                                                                    DOI: 10.1111/j.1752-4571.2008.00045.xSave Citation »Export Citation »E-mail Citation »

                                                                                    Local sources may lack genetic variation leading to poor restoration outcomes. Promotes genetic diversity and high-quality seed to maximize establishment and ability to adapt to environmental change. Provides a cautionary strategy for the mixing of seed provenances to achieve this goal, especially when there is evidence for local adaptation.

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                                                                                    • Harris, James A., Richard J. Hobbs, Eric Higgs, and James Aronson. 2006. Ecological restoration and global climate change. Restoration Ecology 14.2: 170–176.

                                                                                      DOI: 10.1111/j.1526-100X.2006.00136.xSave Citation »Export Citation »E-mail Citation »

                                                                                      Historical reference sites may not reflect ecological reality under current and future climate models; therefore, ecological restoration may need to expand to more functioning ecosystems over historical community assemblages. Genetic variability essential.

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                                                                                      • Havens, Kayri, Pati Vitt, Shannon Still, Andrea T. Kramer, Jeremie B. Fant, and Katherine Schatz. 2015. Seed sourcing for restoration in an era of climate change. Natural Areas Journal 35.1: 122–133.

                                                                                        DOI: 10.3375/043.035.0116Save Citation »Export Citation »E-mail Citation »

                                                                                        Local seed sources may not perform best under climate change conditions. Developing large supplies of “workhorse” species and focusing on collecting seeds from difficult conditions increase the likelihood there is a supply of genetically diverse seeds that can be used.

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                                                                                        • Johnson, Randy, Larry Stritch, Peggy Orwell, Scott Lambert, Matthew E. Horning, and Richard Cronn. 2010. What are the best seed sources for ecosystem restoration on BLM and USFS lands? Native Plants 11.2: 117–131.

                                                                                          DOI: 10.2979/NPJ.2010.11.2.117Save Citation »Export Citation »E-mail Citation »

                                                                                          Restoration of ecosystem services on large-scale, highly disturbed lands using woody and herbaceous species that are regionally appropriate. Incorporation of sufficient genetic variation to adapt to changing environmental conditions is very different from the historical cultivar and plant improvement programs.

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                                                                                          • Jones, Thomas A. 2003. The restoration gene pool concept: Beyond the native versus non-native debate. Restoration Ecology 11.3: 281–290.

                                                                                            DOI: 10.1046/j.1526-100X.2003.00064.xSave Citation »Export Citation »E-mail Citation »

                                                                                            Jones adapts plant breeding plant material concepts to restoration ecology, with four levels of Restoration Gene Pool (RGP) organization based on plant material availability and proposed site conditions. Provides cases where improved cultivate varieties or noninvasive species may be appropriate for restoring ecosystem function as well as metapopulation and multiple origin polycross material.

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                                                                                            • Koskela, Jarkko, François Lefèvre, Silvio Schueler, et al. 2013. Translating conservation genetics into management: Pan-European minimum requirements for dynamic conservation units of forest tree genetic diversity. Biological Conservation 157:39–49.

                                                                                              DOI: 10.1016/j.biocon.2012.07.023Save Citation »Export Citation »E-mail Citation »

                                                                                              Advocates for establishment of managed populations for evolutionary processes (adaptive potential across generations) with native and naturalized species. Minimum viable population estimates based on changes in additive genetic variance rather than allelic variance.

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                                                                                              • US Forest Service. Native Plant Materials.

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                                                                                                This informative US Forest Service website has links to why genetics are important in ecological restoration, plant material and species selection, collecting and processing seed, and nursery methods. Rare plants, pollinators, invasive plants, and the lichen links are also educational.

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                                                                                                • Weeks, Andrew R., Carla M. Sgro, Andrew G. Young, et al. 2011. Assessing the benefits and risks of translocations in changing environments: A genetic perspective. Evolutionary Applications 4.6: 709–725.

                                                                                                  DOI: 10.1111/j.1752-4571.2011.00192.xSave Citation »Export Citation »E-mail Citation »

                                                                                                  Classification of translocation strategies based on specific genetic goals relevant to population conservation under current and predicted environmental changes. The approach helps clarify different types of translocations (genetic rescue, genetic capture, genetic restoration, genetic adaptation) based on overall goals. The authors also weigh the risks of different provenance sourcing mixing and translocation strategies under different scenarios.

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                                                                                                  Life History Traits

                                                                                                  Life history traits have been shown to influence the distribution of genetic variation. With the development and extensive application of molecular markers for population genetic studies, from protein electrophoresis to single nucleotide polymorphic DNA, thousands of published studies have addressed genetic questions across a wide range of plant taxa. A review of 735 woody and herbaceous protein electrophoresis studies, Hamrick and Godt 1996 finds that life form and breeding system was associated with the amount and distribution of genetic diversity. A more recent review of flowering plants with polymorphic sequence data, Glémin, et al. 2006 determines that mating system significantly affected sequence diversity, linkage disequilibrium, selection efficacy, and nucleotide base composition. Vekemans and Hardy 2004 examines associations between life history traits and fine-scale spatial genetic structuring, finding that mating system, life form, and population density affected genetic structure. The genetic structure of many long-lived woody species often does not reflect the contemporary habitat fragmentation boundaries because remnant trees likely represent relics from the pre-disturbance populations (Kramer, et al. 2008). In woody plants, there is a decrease in genetic variation of the remnant stand, but there does not seem to be an increase in the inbreeding coefficient (Vranckx, et al. 2011). Genetic variation of long-lived adult trees in the field is higher than the progeny, representing a possible extinction debt reflecting historical genetic diversity. If empirical data are not available for the plant species of interest, then using life history traits to predict the distribution of genetic variation is a reasonable first step.

                                                                                                  • Glémin, Sylvain, Eric Bazin, and Deborah Charlesworth. 2006. Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proceedings of the Royal Society B 273.1604: 3011–3019.

                                                                                                    DOI: 10.1098/rspb.2006.3657Save Citation »Export Citation »E-mail Citation »

                                                                                                    Mating system significantly affected sequence diversity, linkage disequilibrium, selection efficacy, and base composition.

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                                                                                                    • Hamrick, J. L., and M. J. W. Godt. 1996. Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London: Series B 351.1345: 1291–1298.

                                                                                                      DOI: 10.1098/rstb.1996.0112Save Citation »Export Citation »E-mail Citation »

                                                                                                      Relates five life history traits (breeding system, seed dispersal, life form, geographic range, and taxonomic status) to the distribution of genetic variation.

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                                                                                                      • Kramer, Andrea T., Jennifer L. Ison, Mary V. Ashley, and Henry F. Howe. 2008. The paradox of forest fragmentation genetics. Conservation Biology 22.4: 878–885.

                                                                                                        DOI: 10.111/j.1523-1739.2008.0097.xSave Citation »Export Citation »E-mail Citation »

                                                                                                        Fragmentation boundaries often do not delineate mating populations. Genetic structure of isolated remnant tree populations likely represents living relics of largely unrelated pre-disturbance populations rather than populations with sufficient time to experience drift and inbreeding depression.

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                                                                                                        • Vekemans, Xavier, and Olivier J. Hardy. 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13:921–935.

                                                                                                          DOI: 10.1046/j.1365-294X.2004.02076.xSave Citation »Export Citation »E-mail Citation »

                                                                                                          Reanalyzing data from forty-seven plant species using the “Sp” statistic for assessing fine-scale spatial genetic structure (SGS) revealed that mating system, life form, and population density influenced SGS.

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                                                                                                          • Vranckx, Guy, Hans Jacquemyn, Bart Muys, and Olivier Honnay. 2011. Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conservation Biology 26.2: 228–237.

                                                                                                            DOI: 10.1111/j.1523-1739.2011.01778.xSave Citation »Export Citation »E-mail Citation »

                                                                                                            Woody species showed a decrease in diversity, but not an increase in the inbreeding coefficient. Genetic variation in adult plants in the field was higher than offspring, suggesting a genetic extinction debt and probably reflecting historical genetic diversity in a less fragmented landscape.

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                                                                                                            Moving beyond Neutral Markers

                                                                                                            Selectively neutral molecular markers provide valuable information about important population genetic parameters; however, quantitative genetic traits under selection may provide an ecologically more meaningful story (Hedrick 2004). St. Clair, et al. 2005 shows that some Douglas fir seedling quantitative genetic traits were associated with elevation and cool season temperatures, while others were associated with latitude and summer droughts. Advances in genomic techniques are providing new insight into gene expression and the genetic mechanisms of adaptation (Ouborg, et al. 2010). Studies of model plant species advance our understanding of the genetic control of plant traits under selection (Anderson, et al. 2011). The authors of Pickup, et al. 2012 combine neutral and quantitative genetics, environmental variables, and population size to predict adaptive differentiation in Rutidosis leptorrhynchoides. A meta-analysis study comparing quantitative genetic trait (QST) and neutral marker divergence (FST), Leinonen, et al. 2008 shows that QST values are higher, on average, than FST values, suggesting the importance of natural selection affecting population divergence. The authors also discuss the utility of QST-FST comparisons as a tool for inferring the role of natural selection in population divergence, in addition to potential methodological and interpretational issues with both approaches. Inclusion of quantitative genetic traits under selection and genetic control of these traits from the individual to community dynamics or even ecosystem function has been advocated for conservation genetics (see Ouborg, et al. 2006 and Kramer and Havens 2009).

                                                                                                            • Anderson, Jill T., John H. Willis, and Thomas Mitchell-Olds. 2011. Evolutionary genetics of plant adaptation. Trends in Genetics 27.7: 258–266.

                                                                                                              DOI: 10.1016/j.tig.2011.04.001Save Citation »Export Citation »E-mail Citation »

                                                                                                              Model plant species have advanced our understanding of evolutionary genetics of ecologically critical traits, providing insight into genetic control of plant adaption on ecological and evolutionary scales.

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                                                                                                              • Hedrick, Philip W. 2004. Recent developments in conservation genetics. Forest Ecology and Management 197.1: 3–19.

                                                                                                                DOI: 10.1016/j.foreco.2004.05.002Save Citation »Export Citation »E-mail Citation »

                                                                                                                Increasing numbers of variable molecular markers provide opportunities to assess the distribution of genetic variation across many taxa. Patterns of neutral variation may tell one story while quantitative genetic (adaptive or detrimental) variation may provide an ecologically more meaningful story.

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                                                                                                                • Kramer, Andrea T., and Kayri Havens. 2009. Plant conservation genetics in a changing world. Trends in Plant Science 14.11: 599–607.

                                                                                                                  DOI: 10.1016/j.tplants.2009.08.005Save Citation »Export Citation »E-mail Citation »

                                                                                                                  Advocates for the inclusion of quantitative genetic approaches for assessing adaptive variation. Dynamic seed transfer zones are needed in the increasingly fragmented modern landscape and with changing climatic patterns.

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                                                                                                                  • Leinonen, T., R. B. O’Hara, J. M. Cano, and J. Merilä. 2008. Comparative studies of quantitative trait and neutral marker divergence: A meta-analysis. Journal of Evolutionary Biology 21.1: 1–17.

                                                                                                                    DOI: 10.1111/j.1420-9101.2007.01445.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                    Meta-analysis of fifty species with both QST and FST estimates from plants, vertebrates, invertebrates, and two fungal published studies. The authors found that quantitative trait estimates were higher, on average, than neutral marker divergence and there was a positive association between the QST and FST estimates. They also discuss methodological and interpretational problems with these approaches.

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                                                                                                                    • Ouborg, N. Joop, Cino Pertoldi, Volker Loeschcke, R. (Kuke) Bijlsma, and Phil W. Hedrick. 2010. Conservation genetics in transition to conservation genomics. Trends in Genetics 26.4: 177–187.

                                                                                                                      DOI: 10.1016/j.tig.2010.01.001Save Citation »Export Citation »E-mail Citation »

                                                                                                                      Advances in genomic techniques provide new research opportunities in gene expression, genome wide estimation of neutral and adaptive variation, and genetic mechanisms that translate into an understanding of adaptation and maladaptation.

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                                                                                                                      • Ouborg, N. J., P. Vergeer, and C. Mix. 2006. The rough edges of the conservation genetics paradigm for plants. Journal of Ecology 94.6: 1233–1248.

                                                                                                                        DOI: 10.1111/j.1365-2745.2006.01167.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                        Offers several revisions to better assess genetic issues in plant conservation genetics. Population size and isolation should be treated as separate parameters affecting population genetics in different ways. Advances in functional eco-genomics and multi-trophic level community genetic studies will help advance the science of conservation genetics beyond neutral molecular marker to population genetics of functional genes.

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                                                                                                                        • Pickup, Melinda, David L. Field, David M. Rowell, and Andrew G. Young. 2012. Predicting local adaptation in fragmented plant populations: Implications for restoration genetics. Evolutionary Application 5.8: 913–924.

                                                                                                                          DOI: 10.1111/j.1752-4571.2012.00284.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                          Study on a perennial endemic aster that included neutral (FST) and quantitative (QST) genetic measures. Local adaptation increased with QST and local population size, while low FST and variation in population structure show the importance of gene flow and drift in constraining local adaptation.

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                                                                                                                          • St. Clair, J. Bradley, Nancy L. Mandel, and Kenneth W. Vance-Borland. 2005. Genecology of Douglas fir in western Oregon and Washington. Annals of Botany 96.7: 1199–1214.

                                                                                                                            DOI: 10.1093/aob/mci278Save Citation »Export Citation »E-mail Citation »

                                                                                                                            In this common garden study of Douglas fir seedlings from 1,338 parents from 1,048 locations throughout western Oregon and Washington, the authors show significant quantitative genetic variation in plant performance related to cool season temperatures and summer droughts. This information is used to guide fir propagule selection.

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                                                                                                                            Inbreeding Depression

                                                                                                                            Inbreeding depression is the decrease in plant fitness as a function of crossing among genetically related individuals and has been of interest for many years (see Darwin 2017, originally published in 1876). Classic and modern molecular genetic research indicates that inbreeding depression and heterosis (hybrid vigor) are predominantly caused by recessive deleterious alleles in populations (Charlesworth and Willis 2009). Inbreeding depression can be expressed in captivity (ex situ) and wild populations (Frankham 2005) and has been shown to contribute to population and species extinction (Spielman, et al. 2004). The negative effects, however, appear to be stronger in natural ecological settings (Keller and Waller 2002). Although it is possible for inbred populations to remove these recessive deleterious alleles, purging this genetic load is not a reliable means of reducing inbreeding depression in small and inbred plant populations, says Byers and Waller 1999. Winn, et al. 2011 finds that mixed-mating and outcrossing species have equally high lifetime inbreeding depression and similar inbreeding depression at the seed set, germination, survival to flowering, and growth/reproduction stages. Inbreeding depression is a significant concern in ecological restoration because the genetic quality of the plant material used in the initial planting can have long-term consequences. Chaves, et al. 2011 proposes regressing progeny phenotypic traits (quantitative genetic measures) on population inbreeding coefficients (co-dominant neutral molecular markers) as a means of estimating inbreeding depression in natural plant populations. This information would be helpful for managing the genetic resources in remnant populations as well as informing plant material selection for ecological restoration.

                                                                                                                            • Byers, Diane L., and Donald M. Waller. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30:479–513.

                                                                                                                              DOI: 10.1146/annurev.ecolsys.30.1.479Save Citation »Export Citation »E-mail Citation »

                                                                                                                              The extent of purging genetic load depends on many population and genetic factors. Purging was identified in a limited number of studies. Although populations can purge genetic load under certain circumstances, it is not consistent or effective enough to reliably reduce inbreeding depression in small and inbred populations.

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                                                                                                                              • Charlesworth, Deborah, and John H. Willis. 2009. The genetics of inbreeding depression. Nature Reviews in Genetics 10:783–796.

                                                                                                                                DOI: 10.1038/nrg2664Save Citation »Export Citation »E-mail Citation »

                                                                                                                                Genetics research shows that inbreeding depression is predominantly caused by the presence of recessive deleterious mutations in populations.

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                                                                                                                                • Chaves, Lazáro José, Roland Vencovsky, Rossana Serrato Mendonça Silva, Mariana Pires de Campos Telles, Maria Imaculada Zucchi, and Alexandre Siqueira Guedes Coelho. 2011. Estimating inbreeding depression in natural plant populations using quantitative and molecular data. Conservation Genetics 12.2: 569–576.

                                                                                                                                  DOI: 10.1007/s10592-010-0164-ySave Citation »Export Citation »E-mail Citation »

                                                                                                                                  Proposes a method for estimating apparent inbreeding depression by regression of phenotypic means of progeny on inbreeding coefficient estimated by co-dominant markers. Inbreeding depression indicated in seedling emergence and initial growth traits.

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                                                                                                                                  • Darwin, Charles. 2017. The effects of cross and self fertilization in the vegetable kingdom. London: Routledge.

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                                                                                                                                    Originally published in 1876. Documents a reduction in seed production and plant height when comparing self-fertilization versus cross-fertilization in fifty-seven plant species (inbreeding depression).

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                                                                                                                                    • Frankham, Richard. 2005. Genetics and extinction. Biological Conservation 126.2: 131–140.

                                                                                                                                      DOI: 10.1016/j.biocon.2005.05.002Save Citation »Export Citation »E-mail Citation »

                                                                                                                                      Inbreeding depression occurs in captive and non-captive (wild) species, reduces reproduction and survival, and may contribute to extinction vortex in small populations. Reduced genetic diversity decreases a population’s ability to evolve while increasing genetic load and inbreeding depression through reduced mate availability. Genetic factors contribute to population and species extinction.

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                                                                                                                                      • Keller, Lukas F., and Donald M. Waller. 2002. Inbreeding effects in wild populations. Trends in Ecology & Evolution 17.5: 230–241.

                                                                                                                                        DOI: 10.1016/S0169-5347(02)02489-8Save Citation »Export Citation »E-mail Citation »

                                                                                                                                        Inbreeding depression affects reproductive fitness in bird, mammal, insect, and plant wild populations, negatively impacting population demographic parameters. Negative genetic effects of small population size and isolation in the modern landscape may be lessened with genetic rescue.

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                                                                                                                                        • Spielman, Derek, Barry W. Brook, and Richard Frankham. 2004. Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the United States of America 101.42: 15261–15264.

                                                                                                                                          DOI: 10.1073/pnas.0403809101Save Citation »Export Citation »E-mail Citation »

                                                                                                                                          Meta-analysis comparing 170 threatened and non-threatened related species that found that heterozygosity was lower in threatened species. Negative genetic factors of small populations, loss of genetic variation, and inbreeding depression can contribute to species extinction.

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                                                                                                                                          • Winn, Alice A., Elizabeth Elle, Susan Kalisz, et al. 2011. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65.12: 3339–3359.

                                                                                                                                            DOI: 10.1111/j.1558-5646.2011.01462Save Citation »Export Citation »E-mail Citation »

                                                                                                                                            Compares the magnitude of inbreeding depression (ID) of selfing, mixed, and outcrossing plant species. Mixed-mating and outcrossing species have equally high lifetime ID and similar ID at four life stages.

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                                                                                                                                            Outbreeding Depression

                                                                                                                                            Outbreeding depression is the reduction in fitness of progeny produced from crossing genetically divergent populations. It can be caused by diluting local adaptations (extrinsic form), or from chromosomal mismatches or disrupting locally coadapted gene complexes (intrinsic form). Outbreeding depression caused by a breakup of local adaptation may be evident in the first generation progeny, but multiple generational fitness and backcrosses studies may be needed to document intrinsic outbreeding depression and it can take more generations to recover fitness (see Edmands 2007 and Hufford and Mazer 2003). Frankham, et al. 2011 suggests that outbreeding depression is not likely between populations from similar ecological settings that have been isolated for less than 500 years; the authors conclude that outbreeding depression in recently fragmented populations is much less of a concern than the negative impacts of inbreeding depression and loss of genetic diversity in small isolated populations. A number of studies have shown some degree of outbreeding depression: for example, in studies of herbaceous species, heterosis in F1 progeny and outbreeding depression attributed to epistasis in F2 or F3 backcrosses (Keller, et al. 2000 and Fenster and Galloway 2000). In two studies of shrubs, the authors of Hufford, et al. 2012 and Forrest, et al. 2011 find evidence of a range of fitness consequences, from inbreeding depression to outbreeding depression, depending upon the crossing distances. In these and other studies (Montalvo and Ellstrand 2001), evidence is found of adaptive differentiation among populations, and outbreeding depression was detected in the F1 generation.

                                                                                                                                            • Edmands, Suzanne. 2007. Between a rock and a hard place: Evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16.3: 463–475.

                                                                                                                                              DOI: 10.1111/j.1365-294X.2006.03148.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                              Thoughtful review of outbreeding depression, documenting the need for multiple generation fitness and backcross studies. The author recommends selection of genetically and adaptively similar sources for genetic rescue.

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                                                                                                                                              • Fenster, Charles B., and Laura F. Galloway. 2000. Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae). Conservation Biology 14.5: 1406–1412.

                                                                                                                                                DOI: 10.1046/j.1523-1739.2000.99234.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                Inbreeding and outbreeding depression were investigated in crosses between 100 m and 2,000 m. F1 progeny showed heterosis relative to parentals, while F3 backcrosses suffered outbreeding depression.

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                                                                                                                                                • Forrest, Cairo N., Kym M. Ottewell, Robert J. Whelan, and David J. Ayre. 2011. Tests for inbreeding and outbreeding depression and estimation of population differentiation in the bird-pollinated shrub Grevillea mucronulata. Annals of Botany 108.1: 185–195.

                                                                                                                                                  DOI: 10.1093/aob/mcr100Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                  Microsatellite and pollination study of this perennial, self-incompatible shrub documented inbreeding and outbreeding depression for seed set, seed size, germination, and seedling growth. Optimal crossing distances follow typical bird pollen transfer distances.

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                                                                                                                                                  • Frankham, Richard, Jonathan D. Ballou, Mark D. B. Eldridge, et al. 2011. Predicting the probability of outbreeding depression. Conservation Biology 25.3: 465–475.

                                                                                                                                                    DOI: 10.1111/j.1523-1739.2011.01662.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                    Outbreeding depression was predicted to be low between populations from similar environments, having the same karyotype and isolated for < 500 years. Conversely, outbreeding depression was more likely when populations have fixed chromosome differences, inhabit different environments, or have been isolated > 500 years. Outbreeding depression in recently fragmented populations is less of an issue than the negative impacts of inbreeding depression and loss of genetic diversity.

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                                                                                                                                                    • Hufford, Kristina M., Siegfried L. Krauss, and Erik J. Veneklaas. 2012. Inbreeding and outbreeding depression in Stylidium hispidum: Implications for mixing seed sources for ecological restoration. Ecology and Evolution 2.9: 2262–2273.

                                                                                                                                                      DOI: 10.1002/ece3.302Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                      Outbreeding depression observed in long-distance crosses, inbreeding depression using within-site crosses relative to intermediate crosses. Authors recommend composite seed mixes to be restricted to local provenance zones, with flexible boundaries.

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                                                                                                                                                      • Hufford, Kristina M., and Susan J. Mazer. 2003. Plant ecotypes: Genetic differentiation in the age of ecological restoration. Trends in Ecology & Evolution 18.3: 147–155.

                                                                                                                                                        DOI: 10.1016/S0169-5347(03)00002-8Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                        In this review of the emerging field of restoration genetics, which combines restoration ecology with population genetics, the authors address the revival of quantitative genetic studies (transplant and common garden studies) and molecular markers to predict genetic consequences of seed transfer zones in native plant populations.

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                                                                                                                                                        • Keller, M., J. Kollmann, and P. J. Edwards. 2000. Genetic introgression from distant provenances reduces fitness in local weed populations. Journal of Applied Ecology 37.4: 647–659.

                                                                                                                                                          DOI: 10.1046/j.1365-2664.2000.00517.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                          F1 and F2 backcross hybrids, between local and nonlocal sources of three weedy species, were compared to parental performance in a field experiment. Outbreeding depression was attributed to epistasis for two species. Heterosis observed in F1 for two species but reduced seed mass in F2.

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                                                                                                                                                          • Montalvo, Arlee M., and Norman C. Ellstrand. 2001. Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae). American Journal of Botany 88.2: 258–269.

                                                                                                                                                            DOI: 10.2307/2657017Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                            Authors assessed the potential for outbreeding depression by hybridizing individuals from six different populations of two varieties of Lotus scoparius; they found that mixing genetically differentiated seed sources could lower the fitness of augmented or restored populations. Genetic and environmental similarities of the source population and the proposed transplant sites should be a consideration when selecting plant material.

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                                                                                                                                                            Founder Effects

                                                                                                                                                            Founder effects can occur when a small number of genetic individuals establish a new population and are characterized by low levels of genetic variation. Naturally occurring colonization and population expansion, in the absence of additional gene flow following establishment, can result in a naturally occurring population lacking genetic variation (see Knapp and Connors 1999; Parisod, et al. 2005; and Vandepitte, et al. 2012). Knowledge of the genetic composition of the plant material used in ecological restoration is essential for avoiding founder effects in newly established populations. Robchaux, et al. 1997 finds that multiple outplanting events of the endangered Mauna Kea Silversword from a single source population were effectively from first or subsequent generations from two individual plants. Fant, et al. 2008 finds that the commercially available sources of American beachgrass were genetically monomorphic, as were the restored sites established with these sources. Three of four outcrossing perennial prairie species showed a decrease in genetic variation and loss of rare alleles in restored populations relative to local remnant source populations (Dolan, et al. 2008). Vilas, et al. 2006 demonstrates the negative effects of inbreeding depression on population reintroduction success by experimentally creating populations with different levels of genetic variation and inbreeding. Experimental crosses produced populations with different levels of founder effects while decreased fitness was associated with severe inbreeding (selfing).

                                                                                                                                                            • Dolan, Rebecca W., Deborah L. Marr, and Andrew Schnabel. 2008. Capturing genetic variation during ecological restoration: An example form Kankakee Sands in Indiana. Restoration Ecology 16.3: 386–396.

                                                                                                                                                              DOI: 10.1111/j.1526-100X.2007.00318.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                              Baptisia leucantha, Coreopsis tripteris, and Zizia aurea had lower genetic variation in restored relative to remnant populations, rare alleles were lost, and there were allele frequency differences. Consistent with founder effects in restored populations, but use of local seed sources captured the majority of genetic variations in remnant seed sources.

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                                                                                                                                                              • Fant, Jeremie B., Rebecca M. Holmstrom, Eileen Sirkin, Julie R. Etterson, and Susanne Masi. 2008. Genetic structure of threatened native populations and propagules used for restoration in a clonal species, American beachgrass (Ammophila breviligulata fern.). Restoration Ecology 16.4: 594–603.

                                                                                                                                                                DOI: 10.1111/j.1526-100X.2007.00348.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                Inter-Simple Sequence Repeats (ISSR) study of native, restored, and commercial sources of dune grass. Native populations were genetically different and genetically diverse compared to the commercial releases. Researchers could identify the nonlocal origin material from plantings established almost ten years prior. Founder effects were evident in restored sites using nursery stock.

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                                                                                                                                                                • Knapp, Eric E., and Peter G. Connors. 1999. Genetic consequences of a single-founder population bottleneck in Trifolium amoenum (Fabaceae). American Journal of Botany 86.1: 124–130.

                                                                                                                                                                  DOI: 10.2307/2656961Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                  A population established with a single founder event was less genetically diverse than a large population. Expanding the genetic base of this inland population with a coastal source was not done because of outbreeding depression concerns.

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                                                                                                                                                                  • Parisod, Christain, Charlotte Trippi, and Nicole Galland. 2005. Genetic variability and founder effect in the pitcher plant Sarracenia purpurea (Sarraceniaceae) in populations introduced into Switzerland: From inbreeding to invasion. Annals of Botany 95.2: 277–286.

                                                                                                                                                                    DOI: 10.1093/aob/mci023Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                    Limited regional divergence associated with founder event less than fifty years prior. There was no difference in seed production or seed weight.

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                                                                                                                                                                    • Robchaux, Robert H., Elizabeth A. Friar, and David W. Mount. 1997. Molecular genetic consequences of a population bottleneck associated with reintroduction of the Mauna Kea Silversword (Argyroxiphium sandwicense ssp. Sandwicense [Asteraceae]). Conservation Biology 11.5: 1140–1146.

                                                                                                                                                                      DOI: 10.1046/j.1523-1739.1997.96314.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                      Intermittent outplanting since 1973 yielded 450 established plants from a single source population that were first or subsequent generations from two maternal plants.

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                                                                                                                                                                      • Vandepitte, K., A. S. Gristina, K. DeHert, T. Meekers, and I. Roldan-Ruiz. 2012. Recolonization after habitat restoration leads to decreased genetic variation in populations of a terrestrial orchid. Molecular Ecology 21.17: 4206–4215.

                                                                                                                                                                        DOI: 10.1111/j.1365-294X.2012.05698.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                        Genetic assignment of the Dactylorhiza incarnate documented founder effects in newly established populations. Recurrent founding from few local sources, loss of genetic diversity, and limited divergence among populations indicate founder effects; however, there was no effect on population fitness.

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                                                                                                                                                                        • Vilas, Carlos, Eduardo San Miguel, Rafaela Amaro, and Carlos Garcia. 2006. Relative contribution of inbreeding depression and eroded adaptive diversity to extinction risk in small populations of shore campion. Conservation Biology 20.1: 229–238.

                                                                                                                                                                          DOI: 10.1111/j.1523-1739.2006.00275.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                          Established eighteen populations of Silene littorea with inbred, inbred with mixed, or outcrossed with mixed seeds. Reintroduction success was limited by inbreeding.

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                                                                                                                                                                          Fitness Consequences of Reduced Genetic Variation

                                                                                                                                                                          For both common and rare species, small populations tend to harbor less genetic variation than larger populations (see Honnay and Jacquemyn 2006), which is associated with reduced fitness and long-term population viability (see Reed and Frankham 2003 and Reed 2005). Meta-analyses show positive associations between population size, fitness, and molecular marker genetic variation (Leimu, et al. 2006) and quantitative genetic variation (Willi, et al. 2006). Small populations experienced greater inbreeding depression, reduced fitness, and less genetic variation. A review and synthesis of the ecological consequences of genetic diversity, Hughes, et al. 2008 shows that genetic diversity has ecological consequences on population, community, and ecosystem processes. Significant effects of genetic diversity were found on primary productivity, population recovery following disturbance, interspecific competition, community structure, and fluxes in energy and nutrients. Rogers 2004 cautions against genetic erosion in native plant population due to habitat loss and fragmentation, as well as restoration activities whereby there is a narrowing of genetic diversity through seed selection or nursery practices. However, there are examples of ecological specialists that naturally have low genetic variation and show no evidence of reduced fitness (see Habel and Schmitt 2012).

                                                                                                                                                                          • Habel, Jan Christian, and Thomas Schmitt. 2012. The burden of genetic diversity. Biological Conservation 147.1: 270–274.

                                                                                                                                                                            DOI: 10.1016/j.biocon.2011.11.028Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                            These authors expand on the genetic costs and benefits of species being ecological specialists with naturally low genetic diversity and ecological generalists with high genetic diversity. Adaptation to local conditions may produce highly adapted populations that naturally have low genetic variation but no evidence of reduced fitness (e.g., black mangroves).

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                                                                                                                                                                            • Honnay, Olivier, and Hans Jacquemyn. 2006. Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conservation Biology 21.3: 423–831.

                                                                                                                                                                              DOI: 10.1111/j.1523-1739.2006.00646.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                              Meta-analysis of common and rare plants documented less genetic variation in small populations, relative to large populations. Outcrossing species were more vulnerable than self-compatible species.

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                                                                                                                                                                              • Hughes, A. Randall, Brian D. Inouye, Marc T. J. Johnson, Nora Underwood, and Mark Vellend. 2008. Ecological consequences of genetic diversity. Ecology Letters 11.6: 609–623.

                                                                                                                                                                                DOI: 10.1111/j.1461-0248.2008.01179.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                The first half of this review defines and clarifies the authors’ quantitative/evolutionary genetic approach; it is followed by studies documenting ecological mechanisms for effects of genetic diversity at population, community, and ecosystem levels of organization.

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                                                                                                                                                                                • Leimu, Roosa, Pia Mutikainen, Julia Koricheva, and Markus Fischer. 2006. How general are positive relationships between plant population size, fitness and genetic variation? Journal of Ecology 94.5: 942–952.

                                                                                                                                                                                  DOI: 10.1111/j.1365-2745.2006.01150.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                  The authors found positive relationships among population size, fitness, and genetic variation. Strength and direction of correlations were independent of life-span and size range. Fitness was positively correlated with genetic variation in self-incompatible species, but independent in self-compatible species.

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                                                                                                                                                                                  • Reed, David H. 2005. Relationship between population size and fitness. Conservation Biology 19.2: 563–568.

                                                                                                                                                                                    DOI: 10.1111/j.1523-1739.2005.00444.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                    Finds that population sizes will have to be maintained at < 2,000 individuals to maintain fitness levels for long-term persistence. Long-term population viability is linked to the genetic consequences of population demographics.

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                                                                                                                                                                                    • Reed, David H., and Richard Frankham. 2003. Correlation between fitness and genetic diversity. Conservation Biology 17.1: 230–237.

                                                                                                                                                                                      DOI: 10.1046/j.1523-1739.2003.01236.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                      Heterozygosity, population size, and quantitative genetic variation were positively associated with population fitness. This pattern follows what is predicted based on theory and empirical studies with negative genetic consequences associated with small population size.

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                                                                                                                                                                                      • Rogers, Deborah L. 2004. Genetic erosion: No longer just an agricultural issue. Native Plants Journal 5.2: 112–122.

                                                                                                                                                                                        DOI: 10.2979/NPJ.2004.5.2.112Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                        Rogers explains the importance of genetic erosion in natural ecological systems and the potential of unintentional genetic erosion through plant material selection and propagation practices. Native Plants Journal is a forum for dispersing practical information about planting and growing native plants for conservation, restoration, revegetation, and reclamation activities.

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                                                                                                                                                                                        • Willi, Yvonne, Josh van Buskirk, and Ary A. Hoffmann. 2006. Limits to adaptive potential of small populations. Annual Review of Ecology and Systematics 37:433–458.

                                                                                                                                                                                          DOI: 10.2307/annurev.ecolsys.37.091305.300Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                          Quantitative genetics review of laboratory and field studies. Selection and dispersal accounted for the weak correlation between census size and quantitative genetic traits in natural populations. Suboptimal conditions in damaged habitat and reduced fitness due to inbreeding will negatively affect the population’s ability to adapt.

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                                                                                                                                                                                          Community and Landscape Genetics

                                                                                                                                                                                          With the advances in genomics research, researchers are starting to show how genetic regulation can influence adaptive traits that influence population dynamics and community interactions and drive ecosystem services. Community genetic studies are starting to link gene expression to population and community dynamics, while the field of landscape genetics attempts to establish relationships between adaptive genomic regions and large-scale environmental drivers (see Holderegger, et al. 2010 and Schoville, et al. 2012). Field experiments have shown that increases in seagrass genotypic diversity were associated with increased population growth resistance and resilience to disturbance and had positive effects on the larger community (Procaccini, et al. 2007). A review of crop and natural systems, Tooker and Frank 2012 finds strong evidence explaining how genotypic diversity can improve plant fitness and productivity through niche partitioning among cultivar genotypes and bottom-up control crop pests through “associational resistance.” In an elegant study, the authors of Campbell, et al. 2013 find inbreeding reduced anti-herbivore phytochemical diversity and quantity in Solanum carolinense, lowering plant inducible defenses, resulting in stronger negative herbivory effects on individual plants. Demonstration of the direct and indirect effects of gene expression on individual fitness through ecosystem services reinforces the importance of genetics in ecological systems.

                                                                                                                                                                                          • Campbell, Stuart A., Jennifer S. Thaler, and Andre Kessler. 2013. Plant chemistry underlies herbivore-mediated inbreeding depression in nature. Ecology Letters 16.2: 252–260.

                                                                                                                                                                                            DOI: 10.1111/ele.12036Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                            Inbreeding reduced Solanum carolinense phenolic expression (phytochemical diversity and quantity), lowering plant-induced herbivore defenses. Herbivore damage was greater in inbred plants, suggesting that herbivores could maintain outcrossing mating systems in nature. Reduced ability to respond to herbivores, as a result of inbreeding, will have negative consequences on population and community restoration efforts.

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                                                                                                                                                                                            • Holderegger, Rolf, Dominique Buehler, Felix Gugerli, and Stephanie Manel. 2010. Landscape genetics of plants. Trends in Plant Science 15.12: 675–683.

                                                                                                                                                                                              DOI: 10.1016/j.tplants.2010.09.002Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                              Landscape genetics incorporates population genetics with landscape ecology. Landscape genetics of adaptive genetic variation attempts to establish relationships between adaptive genomic regions and environmental drivers. Landscape genetics will become even more important in restoration, given the potential of shifting species ranges associated with climate change.

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                                                                                                                                                                                              • Procaccini, Gabriele, Jeanine L. Olsen, and Thorsten B. H. Reusch. 2007. Contribution of genetics and genomics to seagrass biology and conservation. Journal of Experimental Marine Biology and Ecology 350.1: 234–259.

                                                                                                                                                                                                DOI: 10.1016/j.jembe.2007.05.035Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                Field experiments showed that increases in seagrass genotypic diversity were associated with increased population growth, resistance and resilience to perturbation, and positive effects on abundance and diversity of the larger community. Reinforces the importance of genetic variation for population stability and community resilience.

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                                                                                                                                                                                                • Schoville, Sean D., Aurelie Bonin, Olivier Francois, Stephane Lobreaux, Christelle Melodelima, and Stephanie Manel. 2012. Adaptive genetic variation on the landscape: Methods and cases. Annual Review of Ecology, Evolution, and Systematics 43:23–43.

                                                                                                                                                                                                  DOI: 10.1146/annurev-ecolsys-110411-160248Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                  This article discusses experimental design and data analysis approaches in landscape genetics. Detection of loci and genomic regions under selection is aided by the use of next-generation sequencing and outlier-detection statistical methods.

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                                                                                                                                                                                                  • Tooker, John F., and Steven D. Frank. 2012. Genotypically diverse cultivar mixtures for insect management and increased crop yields. Journal of Applied Ecology 49.5: 974–985.

                                                                                                                                                                                                    DOI: 10.1111/j.1365-2664.2012.02173.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                    This review includes crop and natural systems to highlight the interactions between plant genotypic variation and community dynamics. Intraspecific plant genetic diversity can improve plant fitness through bottom-up and top-down effects on pest populations and niche partitioning. Trophic-level interactions may be affected by the genetic variation of the component species.

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                                                                                                                                                                                                    Testing Genotypic Effects on Community and Ecosystem Processes

                                                                                                                                                                                                    Ecological restoration affords an opportunity for large-scale field-based experimental testing of ecological theory in the course of restoring functional ecological communities. Booth and Grime 2003 shows that communities with low genotypic diversity lost species faster and became more divergent than more genetically diverse communities. A field study comparing the effects of Oenothera biennis genotypic diversity and species diversity on arthropod diversity and plant productivity, Cook-Patton, et al. 2011 shows increasing genetic diversity or species diversity resulted in an approximately equivalent increase in productivity (niche complementarity). An increase in arthropod diversity was attributed to abundance-driven accumulation with increased genotypic diversity and resource specialization with increased plant species diversity. Inbreeding decreased herbivore resistance, affecting herbivore-plant genotype interactions and potentially community structure (Delphia, et al. 2009). Crawford, et al. 2007 shows Solidago altissima genotype and genetic diversity affected gall abundance, with gall abundance positively associated with arthropod diversity. Seliskar, et al. 2002 demonstrates Spartina alterniflora ecotypic variation affecting microbial community, algal growth, and larval fish abundance in a common garden. Genetic composition of woody species can significantly influence plant-herbivore interactions. Donaldson and Lindroth 2007 finds that plant genotype by environment (nutrients) interactions influenced herbivore performance. Nutrient levels mediated trembling aspen phenolic glycoside defense benefits, which affected herbivore performance. A seminal paper, Whitham, et al. 2003 presents evidence that genetically heritable traits of individual species can influence community and ecosystem functions, which the authors termed “the extended phenotype.” The authors of Whitham, et al. 2007 use their extensive Populus research to develop the genetic connection among population, community, and ecosystem function.

                                                                                                                                                                                                    • Booth, Rosemary, and J. Philip Grime. 2003. Effects of genetic impoverishment on plant community diversity. Journal of Ecology 91.5: 721–730.

                                                                                                                                                                                                      DOI: 10.1046/j.1365-2745.2003.00804.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                      The authors found that communities consisting of a unique set of genotypes became more divergent in species composition and lost species faster than more genetically diverse communities with the same species composition. Communities with single genotype per species saw the greatest divergence. Genetic diversity was associated with community structure.

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                                                                                                                                                                                                      • Cook-Patton, Susan C., Scott J. McArt, Amy L. Parachnowitsch, Jennifer S. Thaler, and Anurag A. Agrawal. 2011. A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92.4: 915–923.

                                                                                                                                                                                                        DOI: 10.1890/10-0999.1Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                        Increasing genotypic diversity of Oenothera biennis or species diversity of old-field plants, resulted in equivalent increase in aboveground primary production (niche complementarity). Arthropod species richness increased with both types of diversity, but the mechanisms and extent differed between genotypic and species diversity treatments. Host plant genetic diversity was as influential to arthropod diversity as plant species diversity.

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                                                                                                                                                                                                        • Crawford, Kerri M., Gregory M. Crutsinger, and Nathan J. Sanders. 2007. Host-plant genotypic diversity mediates the distribution of an ecosystem engineer. Ecology 88.8: 2114–2120.

                                                                                                                                                                                                          DOI: 10.1890/06-1441.1Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                          Solidago altissima genotype and diversity were the best predictor of bunch gall abundance. Galling significantly increases arthropod diversity because these bunch galls may provide refuges from predators, preferential foraging sites, and potential protection from environmental conditions. Documents tri-trophic interactions driven by plant genotype.

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                                                                                                                                                                                                          • Delphia, Casey M., Consuelo M. De Moraes, Andrew G. Stephenson, and Mark C. Mescher. 2009. Inbreeding in horsenettle influences herbivore resistance. Ecological Entomology 34.4: 513–519.

                                                                                                                                                                                                            DOI: 10.1111/j.1365-2311.2009.01097.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                            Herbivore showed greater preference, higher relative growth rate, and total leaf consumption on selfed versus outcrossed horsenettle. Inbreeding decreased herbivore resistance, which can affect plant-herbivore community interactions. Inbreeding negatively affected individual plant fitness by decreasing herbivore resistance, but this was not related to total leaf nitrogen levels.

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                                                                                                                                                                                                            • Donaldson, Jack R., and Richard L. Lindroth. 2007. Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88.3: 729–739.

                                                                                                                                                                                                              DOI: 10.1890/06-0064Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                              Plant chemistry, defoliation, and gypsy moth larval growth were affected by plant genotype, environment, and their interactions. Nutrient levels mediated phenolic glycoside defense benefits, while trees in the low-nutrient treatment experienced less defoliation. This study suggests that spatial and temporal resource variation may influence the defense benefits in tree species.

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                                                                                                                                                                                                              • Seliskar, Denise M., John L. Gallagher, David M. Burdick, and Laurie A. Mutz. 2002. The regulation of ecosystem functions by ecotypic variation in the dominant plant: A Spartina alterniflora salt-marsh case study. Journal of Ecology 90.1: 1–11.

                                                                                                                                                                                                                DOI: 10.1046/j.0022-0477.2001.00632.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                Plants from northern, central, and southern Atlantic coastal marshes retained their home-site growth forms over a five-year common garden experiment in Delaware (central). Ecotype affected microbial community, algal growth, and larval fish abundance. Spartina alterinfloria genetic diversity affects salt marsh ecology at multiple trophic levels.

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                                                                                                                                                                                                                • Whitham, Thomas G., Joseph K. Bailey, Jennifer A. Schweitzer, et al. 2007. A framework for community and ecosystem genetics: From genes to ecosystems. Nature Reviews Genetics 7.7: 510–523.

                                                                                                                                                                                                                  DOI: 10.1038/nrg1877Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                  This review highlights how cottonwood genetics control plant tannins, which affect community (terrestrial, endophytic, and aquatic) and ecosystem services (nitrogen mineralization and aquatic decomposition). This community and ecosystem genetics approach allows us to understand the genetic basis of community and ecosystem processes.

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                                                                                                                                                                                                                  • Whitham, Thomas G., William P. Young, Gregory D. Martinsen, et al. 2003. Community and ecosystem genetics: A consequence of the extended phenotype. Ecology 84.3: 559–573.

                                                                                                                                                                                                                    DOI: 10.1890/0012-9658(2003)084[0559:CAEGAC]2.0.CO;2Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                    Seminal paper describing the new field of community genetics, defining extended phenotype, and arguing for the genetic bases for community heritability. Extended phenotype is the effect of genes at levels of organization above population. Community genetics is an integrative approach to study genes to ecosystems.

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                                                                                                                                                                                                                    Evaluating Success

                                                                                                                                                                                                                    A few studies have attempted to quantify the success of species introduction and restoration efforts. Suding 2011 shows that a third of restoration projects failed, and only 23 percent of projects were successful at reestablishing desired plant community composition. Similarly, a meta-analysis (Godefroid, et al. 2011) of 249 plant species reintroductions worldwide revealed surprising low survival (52 percent), flowering (19 percent), and fruiting (16 percent) rates, with a decrease in performance over time. Establishing populations in protected sites, using transplants rather than seed, drawing on multiple sources of plant material, and having knowledge of the target species genetic variation were associated with increased project success. Transplants are likely to result in greater establishment rates than using seeds; however, direct seeding may be desirable if cost is low and quality seed availability is high (see Guerrant and Kaye 2007). The theoretical cost and benefits of single versus multiple source planting are well established; however, the long-term genetic impact of these seed choices may require careful molecular ecological studies over multiple generations. Godefroid, et al. 2011 suggests that common experimental designs limit the interpretation of plant introduction studies, while Guerrant and Kaye 2007 demonstrates the value of the experimental approach. Drayton and Primack 2012 suggests that inclusion of reproductive success over several generations and publication of what did not work (failures) would advance reintroduction efforts. Complete recovery typically includes species persistence and natural regeneration, while incomplete recovery may be attributed to local and landscape constraints (shifting species distribution, species feedbacks, and legacies of past land use) (Suding 2011). Suding 2011 also promotes restoring ecosystem services rather than site-specific historical populations or communities because these historical systems may not be adapted to the current or future environmental conditions.

                                                                                                                                                                                                                    • Drayton, Brian, and Richard B. Primack. 2012. Success rates for reintroductions of eight perennial plant species after 15 years. Restoration Ecology 20.3: 299–303.

                                                                                                                                                                                                                      DOI: 10.1111/j.1526-100X.2011.00860.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                      Resurveyed eight perennial species fifteen years after establishment in two reserves showed that almost all of the established populations were gone. Reporting both successes and failures in reintroduction experiments will advance the science of restoration ecology, the authors contend. They say that learning what did not work could be as informative as documenting what did, when designing reintroduction projects.

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                                                                                                                                                                                                                      • Godefroid, Sandrine, Carole Piazza, Granziano Rossi, et al. 2011. How successful are plant species reintroductions? Biological Conservation 144.2: 672–682.

                                                                                                                                                                                                                        DOI: 10.1016/j.biocon.2010.10.003Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                        Meta-analysis of 249 plant reintroductions worldwide revealed that survival (52 percent), flowering (19 percent), and fruiting (16 percent) rates were low and declined over time. Suggestions for increasing project success: working within protected sites, establishing seedlings, transplants from multiple populations, better monitoring, and knowledge of the genetic variation of the target species.

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                                                                                                                                                                                                                        • Guerrant, Edward O., and Thomas N. Kaye. 2007. Reintroduction of rare and endangered plants: Common factors, questions and approaches. Australian Journal of Botany 55.3: 362–370.

                                                                                                                                                                                                                          DOI: 10.1071/BT06033Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                          Biological and methodological factors were discussed for ten species reintroductions across a wide range of ecological habitats. These reintroductions were set up as scientific experiments testing specific hypotheses, providing valuable insight into common issues of ecological restoration.

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                                                                                                                                                                                                                          • Suding, Katharine N. 2011. Toward an era of restoration in ecology: Successes, failures, and opportunities ahead. Annual Review of Ecology, Evolution, and Systematics 42:465–487.

                                                                                                                                                                                                                            DOI: 10.1146/annurev-ecolsys-102710-145115Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                            Despite the need for proper evaluation of restoration projects, comprehensive evaluations are rare. Complete recovery typically includes species persistence and natural regeneration, while incomplete recovery is attributed to local/landscape constraints. Suding promotes restoration of ecosystem services, rather than specific ecological communities, because historical reference benchmarks may not be feasible.

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                                                                                                                                                                                                                            Genetic Composition and Diversity in Restored Populations

                                                                                                                                                                                                                            The genetic composition of a restored population may reflect the genetics of the source material and restored populations/communities (although not advised) are sometimes used as seed sources for future restorations. Few studies, however, have empirically characterized the genetic composition of ecological restorations. A study of the endangered Japanese herb Polemonium kiushianum, Yokogawa, et al. 2013 finds that the ex situ populations were genetically different from and less diverse than remnant populations, which the authors attributed to founder effects and possibly genetic drift in the ex situ populations. In contrast, Gustafson, et al. 2002 and Gustafson, et al. 2004a show that restored populations established with multiple local seed sources were genetically similar in genetic diversity to the local remnant sources. This was attributed to the use of multiple source populations and the self-incompatible species breeding system. Cultivated varieties of the perennial native grasses, developed as forage crops and erosion control, were genetically (Gustafson, et al. 2004a) and competitively (Gustafson, et al. 2004b) different from the local remnant and restored populations. Aavik, et al. 2012 finds that genetic diversity was similar between natural and restored populations of Lychnis flos-cuculi established with commercially produced seed; however, inbreeding coefficients were three times higher in the restored populations. Kettle, et al. 2008 documents genetic bottleneck and elevated inbreeding in nursery stocks of the endangered tropical conifer Araucaria nemoros. A comparison of wild and restored Metasequoia glyptostroboides stands, Li, et al. 2005 finds similar levels of genetic diversity, but the genetic structure of the restored populations reflected plant material source selection. Espeland, et al. 2017 discusses the ways restored populations can differ from wild populations when the native seed used comes from agronomic increase on seed farms; genetic diversity or important traits can unintentionally be lost during collection, or due to choices about growing conditions or collection methods. A study of a keystone tree species in Australia where local seed sources were used, Ritchie and Krauss 2012 shows similar genetic diversity among natural and restored populations and their offspring. Paternity analysis revealed complete outcrossing, very low bi-parental inbreeding, and >50 percent of the paternity attributed to sires beyond the local populations. There were no differences in seedling fitness between natural and restored sources. This study demonstrates the importance of incorporating local seed provenance, genetic integration, and offspring performance and is an example of effective genetic resource management in ecological restoration. In addition to the selection or creation of diverse seed mixes, long-term genetic diversity and adaptation to changing conditions is likely to depend on landscape connectivity and migration between restored and wild populations of the species (Aavik and Helm 2018).

                                                                                                                                                                                                                            • Aavik, Tsipe, Peter J. Edwards, Rolf Holderegger, René Graf, and Regula Billeter. 2012. Genetic consequences of using seed mixtures in restoration: A case study of a wetland plant Lychnis flos-cuculi. Biological Conservation 145.1: 195–204.

                                                                                                                                                                                                                              DOI: 10.1016/j.biocon.2011.11.004Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                              Genetic diversity and allelic richness were similar between natural and sown populations; however, inbreeding coefficients were three times higher in sown populations. Source populations affected genetic structure of sown populations.

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                                                                                                                                                                                                                              • Aavik, Tsipe, and Aveliina Helm. 2018. Restoration of plant species and genetic diversity depends on landscape-scale dispersal. In Special issue: Seed dispersal And soil seed banks: Promising sources for ecological restoration. Edited by Péter Török, Aveliina Helm, Kathrin Kiehl, Elise Buisson, and Orsolya Valkó. Restoration Ecology 26.S2:92–102.

                                                                                                                                                                                                                                DOI: 10.1111/rec.12634Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                Long-term genetic diversity in restored populations depends on landscape-scale dispersal. This process is often disrupted, but it is needed to allow natural increases in species richness and self-sustaining, resilient populations.

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                                                                                                                                                                                                                                • Espeland, Erin K., Nancy C. Emery, Kristin L. Mercer, et al. 2017. Evolution of plant materials for ecological restoration: Insights from the applied and basic literature. Journal of Applied Ecology 54.1: 102–115.

                                                                                                                                                                                                                                  DOI: 10.1111/1365-2664.12739Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                  Unintentional genetic sampling during seed collection, as well as during propagation on seed farms, can result in seed sources that vary dramatically from wild populations of the same species. These differences can lower restored population fitness and reduce restoration success. The authors discuss methods for identifying differences using genetic markers or observation, as well as methods to reduce unintentional selection during agronomic increase.

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                                                                                                                                                                                                                                  • Gustafson, Danny J., David J. Gibson, and Daniel L. Nickrent. 2002. Genetic diversity and competitive abilities of Dalea purpura (Fabaceae) from remnant and restored grasslands. International Journal of Plant Science 163.6: 979–990.

                                                                                                                                                                                                                                    DOI: 10.1086/342709Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                    Restored populations established with seeds from multiple local sources had higher genetic diversity than the isolated remnant populations, and genetic relationships reflected restoration professionals’ seed sources. Local plants outcompeted nonlocal plants. Genetic diversity and competitive ability were not associated with size of the source prairie.

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                                                                                                                                                                                                                                    • Gustafson, Danny J., David J. Gibson, and Daniel L. Nickrent. 2004a. Conservation genetics of two co-dominant grass species in an endangered grassland ecosystem. Journal of Applied Ecology 41.2: 389–397.

                                                                                                                                                                                                                                      DOI: 10.1111/j.0021-8901.2004.00904.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                      Genetic diversity was not different between remnant, restored, or cultivated varieties of these obligate outcrossing perennial grasses. Local remnant and restored populations were genetically different from nonlocal remnant and cultivated varieties, while relationships among local remnant and restored populations reflect biogeography and restoration professionals’ sources.

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                                                                                                                                                                                                                                      • Gustafson, Danny J., David J. Gibson, and Daniel L. Nickrent. 2004b. Competitive relationships of Andropogon gerardii (Big Bluestem) from remnant and restored native populations and select cultivated varieties. Functional Ecology 18.3: 451–457.

                                                                                                                                                                                                                                        DOI: 10.1111/j.0269-8463.2004.00850.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                        Glasshouse and field experiments demonstrated plant performance as a function of seed source. Nonlocal plants were less competitive than local plants and cultivars, with even greater differences in relative performance under field conditions. The cultivated varieties had consistently high performance, likely reflecting the directional selection during cultivar development.

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                                                                                                                                                                                                                                        • Kettle, Chris J., Richard A. Ennos, Tanguy Jaffre, Martin Gardner, and Peter M. Hollingsworth. 2008. Cryptic genetic bottleneck during restoration of an endangered tropical conifer. Biological Conservation 141.8: 1953–1961.

                                                                                                                                                                                                                                          DOI: 10.1016/j.biocon.2008.05.00Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                          Authors found cone production is low and highly variable. Nursery populations established from cones collected from adult trees lacked genetic variation, while nursery stock established from cones collected off the forest floor were less genetically diverse than the adult tree population. Maximizing genetic diversity may require sampling established seedlings from the field.

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                                                                                                                                                                                                                                          • Li, Yuan-Yuan, Xioa-Yong Chen, Xin Zhang, Tian-Yi Wu, Hui-Ping Lu, and Yue-Wei Cai. 2005. Genetic differences between wild and artificial populations of Metasequoia glyptostroboides: Implications for species recovery. Conservation Biology 19.1: 224–231.

                                                                                                                                                                                                                                            DOI: 10.1111/j.1523-1739.2005.00025.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                            Genetic diversity of artificial populations was similar to remnant populations. An analysis of allele frequencies (UPGMA) indicated that the artificial populations were more genetically similar to each other than the wild populations, indicating the influence of source on genetic structure.

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                                                                                                                                                                                                                                            • Ritchie, Alison L., and Siegfried L. Krauss. 2012. A genetic assessment of ecological restoration success of Banksia attenuata. Restoration Ecology 20.4:441–449.

                                                                                                                                                                                                                                              DOI: 10.1111/j.1526-100X.2011.00791.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                              Populations established with local seed sources were as genetically diverse as the remnant populations. Obligate outcrossing and low correlated paternity indicated that > 50 percent of the sires originated from beyond the local populations. There were no difference in seedling performance between remnant and restored population sources.

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                                                                                                                                                                                                                                              • Yokogawa, Masashi, Shingo Kaneko, Yoshitaka Takahashi, and Yuji Isagi. 2013. Genetic consequences of rapid population decline and restoration of the critically endangered herb Polemonium kiushianum. Biological Conservation 157:401–408.

                                                                                                                                                                                                                                                DOI: 10.1016/j.biocon.2012.09.010Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                                                Ex situ populations were less genetically diverse and genetically different from the five remaining wild populations. Intrinsic genetic factors are a concern for the remaining wild populations (genetic bottleneck, genetic drift) and ex situ populations (founder effects, genetic drift).

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