Toward a Predictive Framework for Convergent Evolution: Integrating Natural History, Genetic Mechanisms, and Consequences for the Diversity of Life*

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Toward a Predictive Framework for Convergent Evolution: Integrating Natural History, Genetic Mechanisms, and Consequences for the Diversity of Life* vol. 190, supplement the american naturalist august 2017 Symposium Toward a Predictive Framework for Convergent Evolution: Integrating Natural History, Genetic Mechanisms, and Consequences for the Diversity of Life* Anurag A. Agrawal† Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853; and Department of Entomology, Cornell University, Ithaca, New York 14853 abstract: A charm of biology as a scientific discipline is the diversity ical diversity on our planet. The study of convergence is of life. Although this diversity can make laws of biology challenging to part of a program to discover repeated patterns and general discover, several repeated patterns and general principles govern evolu- principles that govern evolutionary diversification. Indeed, tionary diversification. Convergent evolution, the independent evolu- with the advent of non-model-omics, the study of conver- tion of similar phenotypes, has been at the heart of one approach to un- gent evolution is enjoying a new surge of interest, and this derstand generality in the evolutionary process. Yet understanding when symposium and special issue of the American Naturalist and why organismal traits and strategies repeatedly evolve has been a brings together a superb group to address classic and novel central challenge. These issues were the focus of the American Society questions on the topic. of Naturalists Vice Presidential Symposium in 2016 and are the subject fi of this collection of articles. Although naturalists have long made in- Here I de ne convergence as the independent evolution ferences about convergent evolution and its importance, there has been of similar phenotypes. As has been noted many times, the confusion in the interpretation of the pattern of convergence. Does intrigue of convergence was not lost on one of our greatest convergence primarily indicate adaptation or constraint? How often naturalists, Charles Darwin, when he identified traits such should convergence be expected? Are there general principles that as luminescent organs in seemingly distantly related in- would allow us to predict where and when and by what mechanisms sects and pollen packages in distantly related plants. Dar- convergent evolution should occur? What role does natural history “ play in advancing our understanding of general evolutionary princi- win (1859, p. 193) wrote: although the general appearance ples? In this introductory article, I address these questions, review sev- and function of the organ may be the same . some funda- eral generalizations about convergent evolution that have emerged over mental difference can generally be detected . Natural se- the past 15 years, and present a framework for advancing the study and lection . has sometimes modified in very nearly the same interpretation of convergence. Perhaps the most important emerging manner two parts in two organic beings, which owe but lit- conclusion is that the genetic mechanisms of convergent evolution tle of their structure in common to inheritance from the are phylogenetically conserved; that is, more closely related species tend same ancestor.” Darwin recognized that convergent traits to share the same genetic basis of traits, even when independently evolved. Finally, I highlight how the articles in this special issue further are not necessarily identical in all respects and that their evo- develop concepts, methodologies, and case studies at the frontier of our lution was largely independent, although not completely so, understanding of the causes and consequences of convergent evolution. given that all organisms ultimately share a common ancestor. Most convergent evolution falls under the umbrella of Keywords: adaptation, comparative biology, constraint, evolutionary what may be considered “constrained adaptation”—evolu- ecology, phylogenetic ecology, plant-insect interactions. tion that is limited by the strength of natural selection, genetic architecture, and fitness costs and benefits, all of which nar- Introduction row the number of possible evolutionary outcomes. Although convergence is often interpreted as evidence of both adapta- The search for convergent evolution and its causes is one tion and constraint (sagaciously reviewed by Losos [2011]), way to make sense of the wonderfully bewildering biolog- the two processes are intertwined and thus can be difficult to separate. In this context, constraint has been broadly de- * This issue originated as the 2016 Vice Presidential Symposium presented at fined as “restrictions or limitations on the course or outcome the annual meetings of the American Society of Naturalists. † ” “ E-mail: [email protected]. of evolution (Arnold 1992) or, more generally, the unequal ” Am. Nat. 2017. Vol. 190, pp. S1–S12. q 2017 by The University of Chicago. probability of outcomes in evolution (Schwenk 1994/1995). 0003-0147/2017/190S1-57341$15.00. All rights reserved. Issues of constraint will be important in my discussion of con- DOI: 10.1086/692111 vergent evolution, but because of the varied historical use and This content downloaded from 132.236.027.111 on July 22, 2017 05:12:23 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). S2 The American Naturalist abuse of the term (Futuyma 2010), I will frequently use the ganisms subject to the same selection, a critical approach to term “bias” to simply refer to the pattern of unequal probabil- understanding phylogenetic biases in evolution (Petsch- ity of outcome in evolution (table 1). enka et al. 2017; Rosenblum et al. 2017). As Losos (2011) pointed out, repeated trait-environment Convergence has also been at the center of thinking associations are suggestive of convergent adaptation, and about major ecological patterns and their causes. For exam- measures of natural selection and trait function can eluci- ple, Edwards et al. (2017) seek to understand the causes of date the adaptive nature of convergent traits (box 1). None- deciduousness in woody plants, a highly convergent trait theless, such measures do not address the extent to which that defines several global biomes. In some cases, it has been adaptation may be constrained. Many functional traits can hypothesized that convergence occurs at the community be under selection and yet may be limited in how they can level, driving greater similarity of species within a commu- evolve. As will be discussed later in this article, a pattern of nity than would be predicted from their phylogenetic relat- phylogenetic bias in both the degree of convergence and edness (Schluter 1986). In other cases, dissimilarity evolves the underlying mechanistic basis of convergent traits is due to the convergent evolution of community members reshaping our view of constrained adaptation. The challenge into different niches (Gillespie 2004; Losos 2009). Identify- of studying convergence in our era is thus interpreting pat- ing traits that may be involved in community assembly are terns in natural history on phylogenies, with repeated or critical, as such traits are the link between evolutionary his- divergent genetic mechanisms helping to elucidate general tory and ecological outcomes. Together, these approaches issues in evolution. This was the focus of the American So- represent an exciting frontier in the study of convergent ciety of Naturalists Vice Presidential Symposium in 2016. evolution whereby we are able to study the causes and con- In this introductory article, I aim to (1) introduce general sequences of repeated evolutionary change integrating from issues and concepts in the study of convergence and in par- genes to communities. ticular link the study of convergence to its roots in natural history, (2) provide a framework for addressing modern Natural History: The Roots of the Study questions in convergence and summarize the state of the of Convergent Evolution field in terms of progress and open questions, and (3) high- light themes addressed in the subsequent articles in this Natural history concerns the description of organisms (in- special issue. The current growth in studies of convergence cluding their scientific name), their traits (any phenotype has been fueled by increasingly sophisticated modern ana- or description of their genome), location and distribution, lytical tools of comparative biology, the ability to pinpoint and interactions with the biotic and abiotic environment. genetic mechanisms of convergence using molecular biol- Although natural history serves as a foundation for biology, ogy, and the expansion of observational (as opposed to ex- there continues to be controversy about the role that natural perimental) science in the past few decades. While perhaps history should play in advancing knowledge in modern biol- less common, experimental approaches and novel statisti- ogy (Greene 2005). Yet clearly “reciprocal relationships among cal methods in the study of convergence are helping to ex- the growth of robust theory, experimentation, and accurate plain patterns with process (Lenski 2017; Mahler et al. natural history” (Greene 2005, p. 23) are essential for ad- 2017). We are beginning to study the cellular and molecular vancement in our understanding of evolutionary biology. Nat- mechanisms leading to convergence in distantly related or- ural history continues to be an important source of inspira- Table 1: Glossary of terms relevant to this article Adaptive phenotype A trait with a current function maintained by natural selection Constraint Restrictions or limitations
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