Clade-Level Interactions and Macroevolution

by

Tiago B. Quental, Mathias M. Pires

• LAST REVIEWED: 26 May 2023
• LAST MODIFIED: 26 May 2023
• DOI: 10.1093/obo/9780199941728-0147

Introduction

The notion that biotic interactions affect how populations grow or decline and, as a consequence, whether they persist or perish has been central to the development of ecology and evolutionary theory. Darwin framed evolution as the outcome of intraspecific competition and highlighted the roles of interspecific interactions in driving adaptations. Therefore, the role of biotic interactions is well accepted and frequently studied in ecology and evolutionary studies pertaining to one or very few species. A macroevolutionary perspective of how entire clades are affected by other clades, on the other hand, has not been as well documented, nor theoretically explored, as happened with lower-level studies at shallower time scales or fewer species. This article calls clade-level interaction any clade-level outcome, such as changes in speciation and extinction rates, phenotypic trends, or spatial distribution of the clade, that results from interactions among several species from distinct evolutionary lineages. It is important to note that clade-level interactions are large-scale epiphenomena resulting from the interactions among populations of different species at a local scale, but they require a deeper time perspective to be properly documented and studied. The macroevolutionary literature, particularly in paleontology, has been dominated by how abiotic factors might drive biodiversity patterns, but it has become clear that species interactions can play a significant role and, just like in ecology, drive not only the fate of populations but also perhaps of whole clades.

General Overviews

Macroevolution has been popularly viewed as “evolution above the species level” or as “evolution at longer time scales,” but as Hautmann 2020 proposes, it could also be defined as “evolution that is guided by sorting of interspecific variation (as opposed to sorting of intraspecific variation in microevolution).” Hence, the relevance of biotic interactions as macroevolutionary agents rests on showing that changes in speciation, extinction, and morphological evolution of several species can result directly from such interactions. A longstanding question on macroevolution is whether diversity is limited, a scenario typically interpreted to be affected by interspecific interactions. The role of biotic and abiotic factors as drivers of diversification at deep time has been a central theme in macroevolution and has produced the so-called red queen versus court jester debate, which is explored in Barnosky 2001 and Benton 2009. In that sense the “Red Queen hypothesis” proposed in Van Valen 1973 has given species interactions a central role in evolutionary biology. More recently, Voje, et al. 2015 evaluates the role of Van Valen’s “Red Queen Hypothesis” in stimulating debate and theoretical development in evolutionary biology that goes beyond the “Red Queen Hypothesis” itself. Sepkoski 1996 explores in which contexts competitive interactions could lead to the replacement of whole clades by a new ecologically similar and supposedly superior, competitive clade. Vermeij 1994 emphasizes predation as an important driver of macroevolutionary patterns in this review of the escalation hypothesis. Jablonski 2008 highlights that inferring the role of species interactions on macroevolution has been hindered by our inability to properly understand how lower-level mechanisms might translate into macroevolutionary patterns. Still, both paleontologists and neontologists have now accumulated empirical evidence that biotic interactions, clade-level in particular, might have driven changes at longer time scales, affecting diversification dynamics and macroevolutionary trends, as shown in Hembry and Weber 2020. Compilations of studies on clade-level outcomes of interactions as performed in Jablonski 2008 have suggested that both “negative” (competition and predation) and “positive” (mutualisms) ecological interactions can either increase or decrease rates of diversification. Zeng and Wiens 2021 suggests that the lack of previous systematization and quantitative assessment hampered our understanding of general rules for the effect of biotic interactions on diversification rates. This systematic review indicates that positive interactions might preferentially increase diversification rates while negative interactions might preferentially decrease it. Other recent reviews, such as Hembry and Weber 2020 and Fraser, et al. 2021, have also exposed many exciting unanswered questions and, to some extent, fomented the cross talk among paleontologists and neontologists, which is likely to enhance our understanding of the subject.

• Barnosky, A. D. 2001. Distinguishing the effects of the Red Queen and Court Jester on Miocene mammal evolution in the northern Rocky Mountains. Journal of Vertebrate Paleontology 21.1: 172–185.

  DOI: 10.1671/0272-4634(2001)021[0172:DTEOTR]2.0.CO;2

  An empirical study that contrasts biotic and abiotic controls of biodiversity at deep time and argues for a more prominent role for abiotic factors as the main driver of macroevolutionary change at large temporal and spatial scales. Presents the term “Court Jester” to indicate the role of abiotic factors in driving evolution (as a contrast to the Red Queen hypothesis).

• Benton, M. J. 2009. The Red Queen and the Court Jester: Species diversity and the role of biotic and abiotic factors through time. Science 323:728–732.

  DOI: 10.1126/science.1157719

  A critical synthesis questioning the role of biotic interactions in determining diversification at large temporal and spatial scales.

• Fraser, D., L. C. Soul, A. B. Tóth, et al. 2021. Investigating biotic interactions in deep time. Trends in Ecology & Evolution 36.1: 61–75.

  DOI: 10.1016/j.tree.2020.09.001

  Recent review on how paleontological data might help us understand the role of species interactions in driving biodiversity changes in deep time. Reviews recent methodological advances, presents an overview of methods used to study biotic effects on diversification and highlights areas of future work that might be particularly fruitful.

• Hautmann, M. 2020. What is macroevolution? Palaeontology 63.1: 1–11.

  DOI: 10.1111/pala.12465

  Recent opinion piece that presents different definitions of macroevolution and proposes a new one that, according to the author, better justifies the separation between microevolution and macroevolution.

• Hembry, D. H., and M. G. Weber. 2020. Ecological interactions and macroevolution: A new field with old roots. Annual Review of Ecology Evolution and Systematics 51:215–243.

  DOI: 10.1146/annurev-ecolsys-011720-121505

  Recent review that presents a comprehensive historical perspective on the study of the macroevolutionary effects of biotic interactions and examines the overarching questions that remain to be properly investigated.

• Jablonski, D. 2008. Biotic interactions and macroevolution: Extensions and mismatches across scales and levels. Evolution 62.4: 715–739.

  DOI: 10.1111/j.1558-5646.2008.00317.x

  Classical review that discusses how biotic interactions act at different scales to produce macroevolutionary patterns seen at deep time. Although the review is now a few years old, it is very insightful and gives a deep treatment on the subject. It is also a rich source of ideas for further studies.

• Sepkoski, J. J., Jr. 1996. Competition in macroevolution: The double wedge revisited. In Evolutionary paleobiology. Edited by D. Jablonski, D. H. Erwin, and J. H. Lipps, 211–255. Chicago: Univ. of Chicago Press.

  A very didactic book chapter that lays out the assumptions and mechanisms underlying the role of competition on the fate of whole clades as well as what would be the expected biodiversity patterns if clade-level competition is a relevant macroevolutionary force.

• Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1.1: 1–30.

  Uses survivorship curves from several lineages (derived from their fossil record) to present a general pattern that the author calls the “Law of constant extinction”, which suggests that the probability of extinction of a given lineage is independent of its age. Also proposes a mechanism to explain such pattern, the now famous “Red Queen hypothesis,” which implies that the environment (biotic and abiotic) is constantly changing and that an evolutionary advantage in a given taxon within an adaptive zone implies a negative effect in other taxon in the same adaptive zone, characterizing a “zero-sum game.” A very influential paper that, among other things, brought attention to the role of the interspecific interactions on the diversification dynamics.

• Vermeij, G. J. 1994. The evolutionary interaction among species: Selection, escalation, and coevolution. Annual Review of Ecology, Evolution, and Systematics 25:219–236.

  DOI: 10.1146/annurev.es.25.110194.001251

  Review evaluating the plausibility of the hypothesis of escalation, i.e., that selection imposed by natural enemies has driven long-term evolutionary trends.

• Voje, K. L., Ø. H. Holen, L. H. Liow, and N. C. Stenseth. 2015. The role of biotic forces in driving macroevolution: Beyond the Red Queen. Proceedings of the Royal Society B 282.1808: 20150186.

  DOI: 10.1098/rspb.2015.0186

  A very insightful paper that reviews theoretical work (using different approaches, sometimes not explicitly related to macroevolution) related to how biotic interactions might be a relevant macroevolutionary force. Also discusses how different theories (e.g., ecological theory and macroevolutionary theories) and types of data (neontological and paleontological) should be confronted for a better understanding of the long-term effects of biotic interactions. Through the argumentation it confronts these new perspectives with the older, but still very insightful, “Red Queen hypothesis.”

• Zeng Y., and J. J. Wiens. 2021. Species interactions have predictable impacts on diversification. Ecology Letters 24.2: 239–248.

  DOI: 10.1111/ele.13635

  A synthesis paper in which the authors analyze whether different types of ecological interactions have predictable effects over diversification rates. They find that interactions with positive fitness effects, such as mutualism, generally increase diversification rates, whereas interactions with negative fitness effects such as predation (for the prey) and competition generally decrease diversification rates.