Evolutionary Biology Coevolution
Benjamin J. Ridenhour
  • LAST REVIEWED: 01 May 2019
  • LAST MODIFIED: 13 January 2014
  • DOI: 10.1093/obo/9780199941728-0023


Coevolution is most broadly interpreted as two groups of organisms reciprocally influencing the evolution of each other. Groupings can be made at different levels of biological organization and the coevolution of those groups studied (e.g., within or between species, within or between genera, within or between guilds). The study of coevolution is often considered highly multidisciplinary, as it merges many facets of ecological and evolutionary thinking. The concept of coevolution can at least be traced back to On the Origin of Species (London: John Murray, 1859), wherein Darwin describes an “entangled bank” of species interacting and affecting one another’s evolution (this is commonly referred to as the Entangled Bank Hypothesis). Subsequent to the publication of On the Origin and other works from the mid-1800s, the study of coevolution per se was not a focus of biological research until the mid-1900s. The term “coevolution” is sometimes attributed to “Butterflies and Plants: A Study in Coevolution” (Ehrlich and Raven 1964, cited under Early Studies), in which the authors examined the coevolution of butterflies and plants; however, earlier papers that explicitly use the term coevolution exist (e.g., Mode 1958, cited under Early Studies). In the early 1980s, the article “When Is It Coevolution?” (Janzen 1980, cited under General Overviews), sought to distinguish and classify different types of coevolutionary thinking and, more narrowly, define coevolution. Despite this effort, the term coevolution is still utilized in many different ways and is to some degree dependent on the discipline of the publication (e.g., ecology versus evolutionary biology versus systematics). Due to the ubiquity of interactions between species in nature, the implications of the study of coevolution are far reaching. Studies of coevolution focus on many different types of systems, with the common ones being host-pathogen (or parasite), predator-prey, and plant-pollinator interactions. Numerous mechanisms by which coevolution alters the expected evolutionary and ecological dynamics within populations have been identified; many of these mechanisms have been discovered due to research stemming from the geographic mosaic theory in Thompson 1994 (cited under General Overviews). Empirical demonstrations of underlying processes have proven tricky, however, due to difficulties with studying multiple species across landscapes; theoretical studies are therefore common in coevolutionary biology. Despite the difficulty of field studies, it is clear that coevolution is nearly universally important in shaping the diversity of extant biotic communities.

General Overviews

The study of coevolution as a dedicated field of ecology and evolutionary biology is a fairly recent event. Coevolutionary research has accelerated tremendously since the early 1980s, however, and numerous high-quality overviews exist. It is important to recognize a fundamental division between types of coevolutionary work. Janzen 1980 argues that the term coevolution should be strictly used in the case of reciprocal evolutionary change between a pair of species. In order to establish reciprocal evolutionary change, researchers must demonstrate that species exert selective pressure on one another and that those traits under selection then evolve. The second form of coevolution is often referred to as diffuse coevolution. Fox 1988 argues that the selection acting on a species is not strictly pairwise and that multiple species within a biotic community have significant effects on the evolution of any particular trait. Janzen’s definition of coevolution is the one that is typically favored by coevolutionary biologists themselves. Perhaps the most seminal work to coevolution within the past three decades is that performed by John N. Thompson, which culminates with Thompson 2005. This book is a follow-up to Thompson 1994, which popularizes the concept of the Geographic Mosaic Theory. Great effort has been dedicated to investigating the central tenets of the geographic mosaic theory; clear paths to what is known about and how to test the geographic mosaic were described in Gomulkiewicz, et al. 2007. Interests in diffuse coevolutionary processes have recently become increasingly popular as researchers search for feedback loops between ecological and evolutionary processes. In particular, studies of community genetics, like those of Whitham, et al. 2003, examine how the evolution of interactions between species plays a role in determining community structure. Urban and Skelly 2006 extends this concept to the metacommunity level, where more complex processes between communities are considered. Another area in which diffuse coevolutionary processes play a central role is the study of indirect effects within communities. For example, Trait-Mediated Indirect Interactions, explained in Ohgushi, et al. 2012, occur when interactions with a third species modulate the traits controlling the coevolutionary interaction between two other species.


Currently, no professional society is dedicated solely to the study of coevolutionary biology; thus no journals publish studies strictly on this topic. Because of the way in which studies of coevolution typically involve aspects of both evolution and ecology, publications are often found in prominent journals such as Evolution, Ecology, Trends in Ecology and Evolution, American Naturalist, and Journal of Evolutionary Biology. Studies of coevolution often address very important topics related to the assemblies of organisms observed in nature and can appear in top-tier journals such as Science and Nature. Other interdisciplinary journals such as Evolutionary Ecology also regularly publish studies related to coevolution.

Early Studies

The study of coevolution can be traced back to at least the middle of the 1800s. Early studies of coevolution primarily derived from research on plants and their pollinators or predators and their prey. One of the most commonly cited early studies of plant-pollinator coevolution is that of Darwin 1862, an investigation into orchids and their pollinating moths and in particular the notably long spur of the Christmas orchid Angraecum sesquipedale, for which Darwin hypothesized the existence of moth with an equally long proboscis. The moth was later discovered to be the hawk moth Xanthopan morgani. Contemporary to Darwin, Henry Walter Bates (b. 1825–d. 1892) studied mimicry of nontoxic to toxic Amazonian butterflies as a method of defense against predation (what is now known as Batesian mimicry); only slightly later, Johann Friedrich (Fritz) Mueller (b. 1821–d. 1897) studied mimicry systems in which multiple defended prey species mimicked one another to ward off predators (now known as Muellerian mimicry). Pasteur 1982 provides an excellent review of these mimicry systems. Despite these early forays into coevolutionary thinking, coevolutionary research did not began in earnest until the mid-1900s. One such pioneering study is Flor 1955, which examines resistance of certain flax cultivars to rust fungus; this seminal research looks at the effect of genetics on the outcomes of host-pathogen interactions. Arguably the first paper on coevolutionary theory is Mode 1958, which stems directly from Flor’s earlier paper. Ehrlich and Raven 1964 is a seminal article on the coevolution of butterflies and plants and, in particular, hypothesizes that coevolution is a means to the evolution of communities and species diversification. Studies of coevolution began to proliferate during the 1970s and 1980s. By the early 1980s two important books dedicated to the topic of coevolution appeared. The first, Thompson 1982, more narrowly focuses on types and interactions and the pairwise coevolutionary perspective, whereas the edited volume Futuyma and Slatkin 1983 discusses coevolution in broader contexts, such as diffuse coevolution and phylogenetic coevolution.

  • Darwin, C. R. 1862. On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. London: John Murray.

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    One of Darwin’s classic texts on the natural history of plants and pollinators. This book has been released online.

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    • Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: A study in coevolution. Evolution 18:586–608.

      DOI: 10.2307/2406212Save Citation »Export Citation » Share Citation »

      This paper uses butterflies and plants to demonstrate the importance of coevolution and asks several broad questions regarding community evolution. Available online for purchase or by subscription

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      • Flor, H. 1955. Host-parasite interaction in flax rust—Its genetics and other implications. Phytopathology 45:680–685.

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        A seminal paper that established a genetic mechanism—known as the gene-for-gene model—for plants to defend themselves against pathogens.

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        • Futuyma, D. J., and M. Slatkin, eds. 1983. Coevolution. Sunderland, MA: Sinauer.

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          An edited volume that gives broad perspectives on coevolutionary thinking and is edited by highly regarded researchers, with the noted help of other prominent evolutionary biologists from this era.

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          • Mode, C. J. 1958. A mathematical model for the co-evolution of obligate parasites and their hosts. Evolution 12:158–165.

            DOI: 10.2307/2406026Save Citation »Export Citation » Share Citation »

            One of the earliest papers in which coevolutionary dynamics are investigated from a theoretical standpoint. Available online for purchase or by subscription.

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            • Pasteur, G. 1982. A classification review of mimicry systems. Annual Review of Ecology and Systematics 13:169–199.

              DOI: 10.1146/annurev.es.13.110182.001125Save Citation »Export Citation » Share Citation »

              A good review that covers much of what is known and the theory behind mimetic forms and their coevolution. Available online for purchase or by subscription.

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              • Thompson, J. N. 1982. Interaction and coevolution. New York: Wiley.

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                Thompson’s first book on the subject of coevolution; nicely discusses various forms of interactions and the implications of those forms. This book is very much a precursor to Thompson’s more recent books on coevolution.

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                Interspecific Interactions

                Interactions between species are the building blocks of the coevolutionary process. Classification of interactions is usually done on the basis of the fitness consequence of interacting with another species; the fitness consequence can be beneficial, harmful, or neutral. In cases in which the fitness benefit is neutral to one species, coevolution is not truly occurring within the population but might be occurring at a broader scale (see Hotspots and Coldspots); these interactions are called commensal, amensal, or neutral, depending on whether the second species benefits, loses, or is unaffected by interacting, respectively. Mutualisms occur when both species benefit from the interaction and, conversely, competition is the result of both species being harmed by interacting with each other. Finally, if one species benefits while the other suffers, the interaction is considered an antagonism. Lidicker 1979 gives a full discussion of various types of interactions, and Thompson 1982 (cited under Early Studies) discusses interactions from a coevolutionary perspective. For each type of interaction, several critical aspects determine the type of coevolutionary change that is expected; particularly important are the shape of the fitness function and the genetics that control phenotypes. Abrams 2000 discusses the effects of different shapes of fitness functions and refers to these shapes in terms of the “axis of vulnerability” (i.e., the ways in which fitness may be lost). In particular, Abrams refers to either a unidirectional or bidirectional axis of vulnerability. A unidirectional axis of vulnerability represents systems in which there is directional selection against phenotypes and can possibly lead to systems in which phenotypic escalation, also called arms races, occurs. A bidirectional axis of vulnerability represents systems in which there is stabilizing or disruptive selection on phenotypes. Systems of this type are characterized by phenotypic matching (for mutualisms) or phenotypic cycling (for competitions or antagonisms). Several major-gene mechanisms for genetic determination are commonly used for coevolutionary systems. The gene-for-gene model was established in Flor 1955 (cited under Early Studies) as common method for pathogen resistance in plants. Dybdahl and Storfer 2003 elaborates on the matching-alleles model and inverse matching-alleles model to characterize self/nonself recognition and antigen-antibody binding, respectively. Frank 1996 and Parker 1996 discuss why it may be difficult to distinguish between these underlying genetic mechanisms in empirical systems. Aside from those interactions controlled by major genes, Ridenhour and Nuismer 2007 discusses many examples of coevolutionary interactions governed by quantitative phenotypes; these interactions exhibit important differences in terms of dynamics and outcomes.


                Antagonisms are probably the most commonly studied form of coevolutionary interactions, largely because host-pathogen (e.g., Burdon and Thrall 2009) and host-parasite systems (e.g., Morran, et al. 2011), which both have strong public-health and conservation-related implications, fall under this category. Many classic examples of such systems exist for these types of systems. Brodie, et al. 2002 demonstrates how garter snakes have evolved high levels of resistance to deadly tetrodotoxin that is found in elevated levels in their prey, the rough-skinned newt. Toju and Sota 2006 explores similar arms-race dynamics (see Interspecific Interactions) in the coevolution of Japanese camellias and camellia weevils. Other studies of antagonisms display matching dynamics, such as the parsnip–parsnip webworms studied in Zangerl and Berenbaum 2003 or the nest-parasitic cuckoos of Krüger 2007, or cyclical dynamics, like those reported in Morran, et al. 2011 for snails and their parasites. Coevolutionary antagonisms based on chemical defenses of exploited species have been particularly informative regarding the coevolutionary process; Zangerl and Berenbaum 2003 exemplifies such studies. Siepielski and Benkman 2004 is an example in which numerous species play a role in the species-wide coevolutionary dynamics (see Diffuse Coevolution and Trait-Mediated Indirect Interactions). Studies of coevolutionary antagonisms have had far-reaching implications: for example, Morran, et al. 2011 suggests that coevolutionary antagonisms influence the evolution and maintenance of sexual reproduction.

                • Brodie, E. D., Jr., B. J. Ridenhour, and E. D. Brodie III. 2002. The evolutionary response of predators to dangerous prey: Hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067–2082.

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                  This paper shows the magnitude of phenotypic variation created across the US Pacific Northwest due to the coevolutionary process between predator and prey. Available online for purchase or by subscription.

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                  • Burdon, J. J., and P. H. Thrall. 2009. Coevolution of plants and their pathogens in natural habitats. In Special issue: Plant-microbe interactions. Edited by P. J. Hines and L. M. Zahn. Science 324:755–756.

                    DOI: 10.1126/science.1171663Save Citation »Export Citation » Share Citation »

                    Burdon and Thrall have extensively studied coevolutionary metapopulation dynamics, both theoretical and empirical, in plants and pathogens; this is one of the highest-impact papers on their research. Available online for purchase or by subscription.

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                    • Krüger, O. 2007. Cuckoos, cowbirds and hosts: Adaptations, trade-offs and constraints. In Special issue: Towards the artificial cell. Compiled by R. V. Solé, S. Rasmussen, and M. Bedau. Philosophical Transactions B: Biological Sciences 362:1873–1886.

                      DOI: 10.1098/rstb.2006.1849Save Citation »Export Citation » Share Citation »

                      This paper provides interesting insights and directions for the study of brood parasitism systems.

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                      • Morran, L. T., O. G. Schmidt, I. A. Gelarden, R. C. Parrish II, and C. M. Lively. 2011. Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science 333:216–218.

                        DOI: 10.1126/science.1206360Save Citation »Export Citation » Share Citation »

                        Lively, et al. have studied the dynamics of sexual versus asexual New Zealand mud snails vis-à-vis coevolution since the 1980s; this is a nice capstone paper to much of the work. Available online by subscription.

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                        • Siepielski, A. M., and C. W. Benkman. 2004. Interactions among moths, crossbills, squirrels, and lodgepole pine in a geographic selection mosaic. Evolution 58:95–101.

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                          Benkman’s work on crossbills and lodgepole pine has been at the forefront of coevolutionary research; this paper is one of the most important for understanding of the system. Available online for purchase or by subscription

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                          • Toju, H., and T. Sota. 2006. Imbalance of predator and prey armament: Geographic clines in phenotypic interface and natural selection. American Naturalist 167:105–117.

                            DOI: 10.1086/498277Save Citation »Export Citation » Share Citation »

                            Toju and Sota have published numerous articles that document the arms race between Japanese camellia and camellia weevils; this is the original paper that garnered attention for this system. Available online for purchase or by subscription.

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                            • Zangerl, A. R., and M. R. Berenbaum. 2003. Phenotype matching in wild parsnip and parsnip webworms: Causes and consequences. Evolution 57:806–815.

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                              Classic example of plant chemical defense versus herbivores and the coevolutionary response. Berenbaum and Zangerl have many studies on this system. Available online for purchase or by subscription.

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                              Mutualism has been of enormous interest to evolutionary biologists throughout history. Darwin 1862 (cited under Early Studies), which studied orchids and their pollinators, is an example of early research on mutualisms. Other early studies of mutualisms, such as Janzen 1966 on ants and acacias, have been foundational to modern coevolutionary biology. Bronstein 1994 surveys the evolutionary ecology literature and finds that approximately 90 percent of studies of interspecific interactions focused on plant-insect interactions and that, of those studies, roughly 63 percent focused on identifying mutualists. Powell, et al. 2009 suggests that mutualisms between plants and their subterranean mycorrhizal fungi may be one of the most important interactions between all biotic organisms and display a range of forms and evolutionary strategies; in fact, Bronstein, et al. 2006 estimates that approximately 80 percent of flowering plants are involved in mutualisms with mycorrhizal fungi. Studies such as Kerdelhué, et al. 2000 have yielded many classic examples, such as the relationship between figs and their pollinating fig wasps; Mueller, et al. 2005 shows that ants practice “agriculture” by farming fungi that provide antibiotics; Althoff, et al. 2006 has identified that an obligate mutualism has evolved between yuccas and yucca moths. Bronstein, et al. 2006 suggests that many conceptual issues underlying the maintenance of mutualisms still require resolution, in particular, the evolution of “cheaters” (species that once were mutualists but then become antagonists). Brown and Vincent 2008 explores these issues by using game theoretic modeling of different situations like the “Prisoner’s dilemma” or the “Snowdrift game” to represent mutualisms.

                              The Geographic Mosaic Theory

                              Thompson 1994 and Thompson 2005 (both cited under General Overviews) expound the author’s ideas of the geographic mosaic theory, which has perhaps been the most important innovation with regard to our overall understanding of the coevolutionary process. The geographic mosaic theory is made up of a set of “evolutionary hypotheses” and “general ecological predictions.” The general ecological predictions of the geographic mosaic theory are as follows: (1) there will be variation in traits among populations, (2) trait “matching” between species will happen only within communities, and (3) there will be few species-level coevolved traits. Gomulkiewicz, et al. 2007 (cited under General Overviews) discusses how these general ecological predictions are generally upheld by research studies but are not necessarily outcomes unique to the geographic mosaic theory. More interesting are the “evolutionary hypotheses”: (1) different populations will become hotspots and coldspots (see Hotspots and Coldspots) of coevolution, (2) selection mosaics (see Selection Mosaics) will lead to variable evolutionary trajectories across populations, and (3) trait remixing (see Trait Remixing) will alter the spatial distribution of coevolving traits. Kawecki and Ebert 2004 explores the issues surrounding a central question of (co)evolutionary biology, namely, whether species become locally adapted. To this end, the authors of Nuismer 2006 and Gandon and Nuismer 2009 have performed theoretical studies to consider the effects of coevolution on local adaptation. Generally, theory shows that selection mosaics and trait remixing have important—and sometimes nonintuitive—effects with regard to local adaptation. Other important conclusions have resulted from the study of the geographic mosaic theory. For example, using experimental evolution techniques, Brockhurst, et al. 2003 has demonstrated that coevolution can alter the tempo of evolution and, in particular, speed up evolution. Likewise, classic studies of host-parasite coevolution, such as Jokela, et al. 2009, demonstrate that sexual reproduction of organisms can be favored by coevolution, despite being costly. Thompson 2009 enumerates some of the most important advances that have been brought about by studying the geographic mosaic theory.

                              • Brockhurst, M. A., A. D. Morgan, P. B. Rainey, and A. Buckling. 2003. Population mixing accelerates coevolution. Ecology Letters 6:975–979.

                                DOI: 10.1046/j.1461-0248.2003.00531.xSave Citation »Export Citation » Share Citation »

                                This paper discusses how geographic mosaics might accelerate the rate at which evolution occurs. Available online for purchase or by subscription.

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                                • Gandon, S., and S. L. Nuismer. 2009. Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. American Naturalist 173:212–224.

                                  DOI: 10.1086/593706Save Citation »Export Citation » Share Citation »

                                  A comprehensive study that shows how different microevolutionary forces affect local adaptation in coevolutionary systems. Available online for purchase or by subscription.

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                                  • Jokela, J., M. F. Dybdahl, and C. M. Lively. 2009. The maintenance of sex, clonal dynamics, and host–parasite coevolution in a mixed population of sexual and asexual snails. In Special issue: The Evolution of Sex; Recent Resolutions and Remaining Riddles; A Symposium. Organized by S. P. Otto. American Naturalist 174.S1: S43–S53.

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                                    Paper discussing Red Queen dynamics in maintaining sexual reproduction in certain populations of New Zealand mud snails. Available online for purchase or by subscription.

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                                    • Kawecki, T., and D. Ebert. 2004. Conceptual issues in local adaptation. Ecology Letters 7:1225–1241.

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

                                      This paper gives different ways in which local adaptation can be conceptualized, particularly from the viewpoint of host-parasite coevolution.

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                                      • Nuismer, S. 2006. Parasite local adaptation in a geographic mosaic. Evolution 60:24–30.

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                                        A paper that demonstrates the importance of geographically variable selection in interspecific interactions. Available online for purchase or by subscription.

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                                        • Thompson, J. N. 2009. The coevolving web of life. American Naturalist 173:125–140.

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                                          Thompson’s presidential address to the American Society of Naturalists in which he addresses the major gains and failures in our understanding of coevolutionary biology. Available online for purchase or by subscription.

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                                          Hotspots and Coldspots

                                          Hotspots and coldspots of coevolution are one of the three fundamental evolutionary processes of the geographic mosaic theory (Thompson 1994 and Thompson 2005, cited under General Overviews). Hotspots are populations in which reciprocal evolution (per Janzen 1980, cited under General Overviews) is occurring; coldspots are, put simply, populations that are not hotspots. Gomulkiewicz, et al. 2007 (cited under General Overviews) identifies a common misconception that a gradient exists between hotspots and coldspots, and that coldspots are areas where reciprocal selection is weak; even areas where (reciprocal) selective forces are weak are considered hotspots. In order to establish that natural selection is a result of interacting with another species, special techniques such as selective source analysis, expounded in Ridenhour 2005, or testing for diffuse coevolution, as explained in Iwao and Rausher 1997 (cited under Diffuse Coevolution), are required. Vogwill, et al. 2009 and Thompson, et al. 2002 shows that hotspots and coldspots play an important role in the rate of evolution and local adaptation within coevolving species. The causes of hotspots and coldspots can be quite diverse. For example, Benkman, et al. 2001 finds that crossbills have little or no selective effects on lodgepole pine when a third species, squirrels, is present to act as pine cone predators (thus creating a coldspot). As another example, Hochberg and van Baalen 1998 shows that differences in productivity among population can also lead to the formation of hotspots and coldspots. In contrast to the broad geographic scale of hotspots and coldspots observed in crossbills and other systems, Laine 2006 demonstrates that hotspots and coldspots can occur at very localized scales.

                                          Selection Mosaics

                                          Selection mosaics are perhaps the most novel concept within the framework of the geographic mosaic theory. A selection mosaic is not simply the presence of variability in the strength of coevolutionary selection across different populations; rather, it is that fitness outcomes of a specific interaction vary. Thompson 2005 (cited under General Overviews) explains selection mosaics as being a genotype × genotype × environment (G × G × E) interaction. Gomulkiewicz, et al. 2007 (cited under General Overviews) provides an illustration a G × G × E interaction: consider an individual having genotype A of species 1 who interacts with an individual having genotype B of species 2. In one population when A interacts with B it produces some fitness for both species; however, if there is a selection mosaic A interacting with B, it produces a completely different fitness outcome in other populations. The difference in fitness outcomes between the two populations is a result of the environment (E); Thompson 2009 (cited under Geographic Mosaic Theory) points out that this environment is often the biotic environment (i.e., the community in which an interaction takes place (see Diffuse Coevolution). Thus presence or absence of tertiary species can lead to the formation of selection mosaics, such as described in Benkman 1999. Detecting G × G × E interactions is not a simple task, but it has been proposed that methods such as those developed in Kirkpatrick and Heckman 1989 or Kingsolver, et al. 2001 could possibly be put to such a use. Several studies have shown strong potential for the existence of a selection mosaic. Most of these studies have involved some form of experimental manipulation or laboratory-based experimental designs. For example, Rudgers and Strauss 2004 demonstrates geographically variable selection by using manipulating ant interactions with cotton across population; similarly, Piculell, et al. 2008 uses a greenhouse experimental design to detect a possible selection mosaic in an ectomycorrhizal symbiosis. Because of the difficulty of testing for G × G × E interactions, fewer studies have attempted to look at selection mosaics in situ, but some examples do exist. Specifically, a study of garter snakes and newts in Hanifin, et al. 2008 suggests that the nature of coevolutionary selection is different in populations in which predator or prey phenotypes are highly exaggerated, and Benkman 1999 hypothesizes optimal beak sizes depend on whether Tamiasciurus is present in a population.

                                          • Benkman, C. W. 1999. The selection mosaic and diversifying coevolution between crossbills and lodgepole pine. American Naturalist 153:S75–S91.

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                                            This paper comes from the very worthwhile 1999 American Naturalist special issue on coevolution; the research presented shows strong potential for the presence of a selection mosaic. Available online for purchase or by subscription.

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                                            • Hanifin, C. T., E. D. Brodie Jr., and E. D. Brodie III. 2008. Phenotypic mismatches reveal escape from arms-race coevolution. PLoS Biology 6.3: e60.

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                                              Reports that populations in which selection pressure has changed due to extreme phenotypic exaggeration in either garter snake or newts suggests the presence of selection mosaic.

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                                              • Kingsolver, J. G., R. Gomulkiewicz, and P. A. Carter. 2001. Variation, selection and evolution of function-valued traits. Genetica 112–113:87–104.

                                                DOI: 10.1023/A:1013323318612Save Citation »Export Citation » Share Citation »

                                                Because traits involved in a G x G x E interaction can be thought of as a function-valued trait (in which the resulting phenotype is a result of another G x E interaction), the methods for studying function-valued traits might successfully be applied to selection mosaics. Available online for purchase or by subscription.

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                                                • Kirkpatrick, M., and N. Heckman. 1989. A quantitative genetic model for growth, shape, reaction norms, and other infinite-dimensional characters. Journal of Mathematical Biology 27:429–450.

                                                  DOI: 10.1007/BF00290638Save Citation »Export Citation » Share Citation »

                                                  Selection mosaics are essentially a form of reaction norm; therefore, the methods put forward in this paper for studying selection norms apply to the study of selection mosaics. Available online for purchase or by subscription.

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                                                  • Piculell, B. J., J. D. J. Hoeksema, and J. N. Thompson. 2008. Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. BioMed Central (BMC) Biology 6:23.

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                                                    Perhaps the best evidence of the selection mosaics available. The authors performed a specific experimental designed to look for evidence of G x G x E interactions in interactions with mycorrhizal fungi.

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                                                    • Rudgers, J. A., and S. Y. Strauss. 2004. A selection mosaic in the facultative mutualism between ants and wild cotton. Proceedings of the Royal Society: Biological Sciences 271:2481–2488.

                                                      DOI: 10.1098/rspb.2004.2900Save Citation »Export Citation » Share Citation »

                                                      By using manipulations of extrafloral nectaries and ant exclusion treatments, this paper hints at the presence of a selection mosaic in this coevolutionary system.

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                                                      Trait Remixing

                                                      Trait remixing is probably the most easily demonstrable and least controversial aspect of the geographic mosaic theory. Factors that lead to trait remixing are any nonselective forces that can cause the evolution of traits across metapopulations. Therefore, microevolutionary forces such as gene flow, mutation, and genetic drift can all be sources of trait remixing. Of these microevolutionary forces, the easiest to study empirically is gene flow through the use of population genetic/genomic techniques such as fragment analysis or restriction site associated DNA (RAD) tagging. Many studies, such as Dybdahl and Lively 1996 on gene flow in snails and their castrating trematode parasite, or Ridenhour, et al. 2007 on gene flow in coevolving garter snakes and newts, have demonstrated that patterns of gene flow are important to the coevolutionary process. Nuismer, et al. 1999 studies gene flow extensively from a theoretical standpoint. Particularly interesting results produced by the authors of Gandon and Michalakis 2002 demonstrate that gene flow, traditionally considered to be a maladaptive force, can improve the opportunity for local adaptation by introducing novel genetic variants. Empirical demonstrations of these effects exist, such as Thrall, et al. 2002, which examines the effects of gene flow on local adaptation in a plant-pathogen system. Studies of the effects of mutation or genetic drift on coevolution have been limited; most studies of these factors have either been performed by using experimental evolution or by theory. Important results have stemmed from these studies, however. For example, Hall, et al. 2011 shows that coevolution can lead to specific mutations that lead to the evolution of generalism in pathogens, and Schulte, et al. 2010 shows that coevolution may speed up the process of reciprocal adaptation via increases in mutation rates. Studies of genetic drift on the coevolutionary process are rare and currently theoretical in nature, but have also led to important conclusions. Examples of these articles include Nuismer, et al. 2010 (cited under Summary), which looks at coevolution-driven patterns of phenotypic diversity, and Gandon and Nuismer 2009 (cited under Geographic Mosaic Theory) which investigates the effect of genetic drift on local adaptation. In addition to the previously mentioned microevolutionary forces, Alexander, et al. 1996 shows that metapopulation dynamics such as extinction and recolonization also play an important role in shaping spatial patterns of genetic and phenotypic diversity in coevolutionary interactions.

                                                      Diffuse Coevolution

                                                      The study of coevolution can essentially be broken down into two broad categories: pairwise and diffuse coevolution (see General Overviews). The difference between these two branches of coevolutionary thinking comes down to a debate about reductionism, as described in Strauss and Irwin 2004. With pairwise coevolution, the research is broken down to the most basic unit of an interaction between species. In contrast, diffuse coevolution argues that interactions among all the species within a community must be studied to understand evolutionary and ecological dynamics. While pairwise coevolution has garnered more attention from researchers (particularly since the Thompson published his work on the Geographic Mosaic Theory), the study of diffuse coevolution has a long history, and there has been recent renewed interest in this topic. The study of butterflies in Ehrlich and Raven 1964 (cited under Early Studies) focuses on the evolution of communities with respect to plant-herbivore interactions and, more specifically, how such interactions might generate diversity (see Coevolution and Diversity); this is a clear example of a diffuse coevolutionary process. Similarly, a majority of the studies of diffuse coevolution have focused on plant-insect interactions. Atsatt and O’Dowd 1976 addresses how different plants within a community can coevolve to defend themselves from herbivory by pests. One general hypothesis from this literature is that plants should evolve defenses that protect them from a suite of enemies. To explore this hypothesis, Leimu and Koricheva 2006 presents a comprehensive meta-analysis of published literature that considers the correlations between resistances to multiple pest species. This work finds that indeed plant resistance often defends against multiple species. Studies of coevolution at broad levels of biological organization, such as the study of fly-pollinated plants in Anderson and Johnson 2009, still appear regularly in the literature. The study of diffuse coevolution has required the development of novel theoretical tools such as the models in Levin, et al. 1990 and a novel type of selection analysis, like that expounded by Iwao and Rausher 1997, to detect diffuse coevolution. Much theoretical work has focused on understanding how indirect effects (as compared to pairwise effects) between species operate: Wootton 1994 provides a general introduction to indirect species interactions. Classically, indirect effects in diffuse coevolution were studied by understanding how changing species densities in a community affects interspecific interactions; these are so-called density-mediated indirect effects (DMIIs) or are sometimes referred to as trophic cascades. In contrast to this classical viewpoint, indirect effects can also be trait mediated, as shown by Abrams 1995. Trait-Mediated Indirect Interactions have closer ties to pairwise coevolution yet still address the issue of multispecies interactions.

                                                      Trait-Mediated Indirect Interactions

                                                      Ridenhour and Nuismer 2012 discusses the emerging area of trait-mediated indirect interactions (TMIIs), which has many applications to the study of coevolution. TMIIs are the result of a third species affecting a trait involved in a pairwise interspecific interaction. The concept of a TMII relates directly to that of Selection Mosaics, which are defined by G × G × E interactions. A TMII is essentially a case in which a third species is the environment (E), which then alters the G x G interaction between two species. Wootton 1994 and Abrams 1995 (cited under Diffuse Coevolution) provide general introductions to TMIIs. Empirical demonstrations of TMIIs began being published by the late 1990s. Two examples of such studies are Peacor and Werner 1997 on trophic effects in aquatic food webs and Abrahamson and Weis 1997 on trophic effects in the interactions between goldenrod, gallmaking wasps, and birds. Schmitz, et al. 2004 suggests that understanding TMIIs may be more important to overall community dynamics than studying density-mediated indirect effects. Currently, the effects of TMIIs have been studied in a number of different settings, such as in Wolfe, et al. 2005, a study of mycorrhizal mutualisms affecting aboveground mutualisms in plants; in Lau 2012, a study of biological invasion by exotics altering the evolution of native plants; and a study of plants driving bottom-up effects on insect communities, as shown by Price, et al. 2005. Ohgushi 2005 reviews many different plant-insect communities and how indirect effects play important roles in shaping those communities. As a more general reference, Ohgushi, et al. 2012 (cited under General Overviews) is an edited volume that contains a section specifically devoted to coevolution and has several chapters with detailed examples of how TMIIs are important to coevolutionary interactions.

                                                      Coevolution and Diversity

                                                      Coevolutionary interactions have long been assumed to generate diversity in a phylogenetic context. Ehrlich and Raven 1964 (cited under Early Studies) concludes that the diversity that is observed in butterflies is a result of coevolution with the diversity of dicotyledons (butterflies are primarily herbivores of dicotyledons, which use secondary compounds as a defense mechanism). Ehrlich and Raven’s proposed model of coevolutionary diversity has been applied to other groups of organisms, perhaps most notably in Farrell 1998, which shows similar patterns of diversification in beetles with plants. Similar to Ehrlich and Raven’s pioneering study, Van Valen 1973–1976 proposes the Red Queen Hypothesis to explain the patterns of species diversity observed over geologic time (on the basis of fossil records) in various taxa. The Red Queen Hypothesis, as originally stated, was the idea that lineages are gained and lost because of reciprocal responses in hosts and parasites; the Red Queen Hypothesis has become a commonly cited principle in coevolution but is now more generally used to represent negative frequency-dependent selection in antagonistic interactions. More recently, Schluter 2000 has proposed that competitive interactions between species can lead to diversification by ecological character displacement; the author supports this proposal with research on diversification of different forms of threespine stickleback fish. Theoretical studies, such as in Doebeli and Dieckmann 2000, have also demonstrated that, under the appropriate circumstances, coevolutionary interactions between species can lead to diversification. Despite the number of studies that have hypothesized that coevolutionary interactions have led to greater biotic diversity, distinguishing these hypotheses from those that do not involve coevolution is difficult. For example, distinguishing between a hypothesis of cospeciation, in which two species share phylogenetic patterns because of factors extrinsic to an interaction, and coevolution can be particularly difficult (however, Diffuse Coevolution could still potentially lead to cospeciation). As examples of this difficulty, a hypothesis of cospeciation has been used in Clayton, et al. 2003 to explain phylogenetic relationships of feather lice and in Ricklefs, et al. 2004 to explain observed patterns of host switching in avian malaria. Similarly, a recent theoretical study in Yoder and Nuismer 2010 concludes that only certain types of coevolutionary interactions—in particular those in which phenotype matching (see Interspecific Interactions) is involved—lead to diversification; these authors therefore call for a reassessment of the general hypothesis that coevolution is a driver of biotic diversity.

                                                      • Clayton, D. H., S. E. Bush, B. M. Goates, and K. P. Johnson. 2003. Host defense reinforces host–parasite cospeciation. Proceedings of the National Academy of Sciences of the United States of America 100:15694–15699.

                                                        DOI: 10.1073/pnas.2533751100Save Citation »Export Citation » Share Citation »

                                                        Clayton’s studies of bird feather lice have become classics in the field of coevolution. This particular study focuses on shared phylogenetic patterns between feather lice and pigeons/doves.

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                                                        • Doebeli, M., and U. Dieckmann. 2000. Evolutionary branching and sympatric speciation caused by different types of ecological interactions. In Special issue: Species interactions and adaptive radiation; A symposium. Organized by D. Schluter. American Naturalist 156:S77–S101.

                                                          DOI: 10.1086/303417Save Citation »Export Citation » Share Citation »

                                                          This article is from the same special issue of American Naturalist as Schluter 2000. The authors use adaptive dynamics to look at the potential for various forms of interactions (e.g., mutualisms, predator-prey) to lead to speciation. Available online for purchase or by subscription.

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                                                          • Farrell, B. D. 1998. “Inordinate fondness” explained: Why are there so many beetles? Science 281:555–559.

                                                            DOI: 10.1126/science.281.5376.555Save Citation »Export Citation » Share Citation »

                                                            A modern reexamination that supports Ehrlich and Raven’s earlier work on the diversity of plants and insects (Ehrlich and Raven 1964, cited under Early Studies). Farrell uses beetle diversity, historically noted by Theodosius Dobzhansky (b. 1900–d. 1975), as a comparator. Available online by subscription.

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                                                            • Ricklefs, R. E., S. M. Fallon, and E. Bermingham. 2004. Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53:111–119.

                                                              DOI: 10.1080/10635150490264987Save Citation »Export Citation » Share Citation »

                                                              An interesting cospeciation study that not only examines this hypothesis but also investigates different statistical methods of testing for cospeciation. Available online for purchase or by subscription.

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                                                              • Schluter, D. 2000. Ecological character displacement in adaptive radiation. In Special issue: Species interactions and adaptive radiation; A symposium. Organized by D. Schluter. American Naturalist 156:S4–S16.

                                                                DOI: 10.1086/303412Save Citation »Export Citation » Share Citation »

                                                                A very good paper explaining Schluter’s hypothesis regarding competitive displacement of species; this article is part of a special issue that is very informative. Article available online for purchase or by subscription.

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                                                                • Van Valen, L. 1973–1976. A new evolutionary law. Evolutionary Theory 1:1–30.

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                                                                  A classic but difficult read; Van Valen created the journal Evolutionary Theory in order to publish this paper. Articles from the journal are freely available online.

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                                                                  • Yoder, J. B., and S. L. Nuismer. 2010. When does coevolution promote diversification? American Naturalist 176:802–817.

                                                                    DOI: 10.1086/657048Save Citation »Export Citation » Share Citation »

                                                                    This paper performs a similar analysis to that of Doebeli and Dieckman 2000, but the authors use traditional quantitative genetic style models and arrive at the conclusion that many types of interactions do not promote diversity. Available online for purchase or by subscription.

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                                                                    The study of coevolutionary interactions has a long and rich history that dates back at least until the mid-1800s, when Darwin, Bates, and Mueller separately published studies on plant-pollinator interactions and mimicry (see Early Studies). The study of coevolutionary biology per se began in earnest in the mid-1900s but with the largest boom in interest to come in the early 1980s when seminal publications such as Janzen 1980 (cited under General Overviews), Thompson 1982 (cited under Early Studies), Futuyma and Slatkin 1983 (cited under Early Studies), and Fox 1988 (cited under General Overviews) began to shape the formal study of coevolutionary systems. The Geographic Mosaic Theory of coevolution (Thompson 1994 and Thompson 2005, cited under General Overviews) stimulated even greater research interest in coevolution, starting in the mid-1990s. Work done since that time has established many important and sometimes nonintuitive effects that result when species coevolve. Clearly, coevolution may be one of the most import processes in biology, so much so that Thompson 2009 (cited under Geographic Mosaic Theory) advocates that every biology student should be taught several fundamental points regarding coevolution. Despite the great deal of effort that has been put into studying coevolution, empirical tests of many important hypotheses still need to be performed (such as for the presence of Selection Mosaics). Furthermore, some recent studies, such as Nuismer, et al. 2010 and Mueller, et al. 2008, Yoder and Nuismer 2010 (cited under Coevolution and Diversity), and Gomulkiewicz, et al. 2007 (cited under General Overviews), have called for critical reevaluation of many of empirical studies of coevolution, with a more critical look at the actual underlying evolutionary process and less reliance on observed patterns. Finally, studies of Diffuse Coevolution and pairwise coevolution have traditionally been treated separately. However with further investigation of many important interactions, it has become increasingly clear that a more integrated community-level approach that incorporates both diffuse and pairwise coevolution is on the horizon, as discussed in Irschick, et al. 2007. Nowhere is this future more evident than in the confluence of concepts like Trait-Mediated Indirect Interactions and community genetics/genomics with the underlying tenets of the geographic mosaic theory. Disentangling Darwin’s entangled bank of interacting species—which we now know determines the composition and dynamics of biotic communities—will most likely occupy researchers for generations to come.

                                                                    • Irschick, D., J. K. Bailey, J. A. Schweitzer, J. F. Husak, and J. J. Meyers. 2007. New directions for studying selection in nature: Studies of performance and communities. Physiological and Biochemical Zoology 80:557–567.

                                                                      DOI: 10.1086/521203Save Citation »Export Citation » Share Citation »

                                                                      A study that reviews literature on selection and indirect effects within communities and makes specific proposals about how studies of community (co)evolution can successfully be performed in the future. Available online for purchase or by subscription.

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                                                                      • Mueller, U. G., D. Dash, C. Rabeling, and A. Rodrigues. 2008. Coevolution between attine ants and actinomycete bacteria: A reevaluation. Evolution 62:2894–2912.

                                                                        DOI: 10.1111/j.1558-5646.2008.00501.xSave Citation »Export Citation » Share Citation »

                                                                        A review of the agricultural practices of ants that concludes that there is currently not enough evidence to support a hypothesis of coevolution between attine ants and bacteria. Available online for purchase or by subscription.

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                                                                        • Nuismer, S. L., R. Gomulkiewicz, and B. J. Ridenhour. 2010. When is correlation coevolution? American Naturalist 175:525–537.

                                                                          DOI: 10.1086/651591Save Citation »Export Citation » Share Citation »

                                                                          A theoretical study showing that correlation between phenotypes of interacting species can arise for reasons that are not related to coevolution. Available online for purchase or by subscription.

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