Integrating natural history collections and comparative genomics to study royalsocietypublishing.org/journal/rstb the genetic architecture of convergent evolution Review Sangeet Lamichhaney1,2, Daren C. Card1,2,4, Phil Grayson1,2, Joa˜o F. R. Tonini1,2, Gustavo A. Bravo1,2, Kathrin Na¨pflin1,2, Cite this article: Lamichhaney S et al. 2019 1,2 5,6 7 Integrating natural history collections Flavia Termignoni-Garcia , Christopher Torres , Frank Burbrink , and comparative genomics to study Julia A. Clarke5,6, Timothy B. Sackton3 and Scott V. Edwards1,2 the genetic architecture of convergent 1Department of Organismic and Evolutionary Biology, 2Museum of Comparative Zoology, and 3Informatics evolution. Phil. Trans. R. Soc. B 374: 20180248. Group, Harvard University, Cambridge, MA 02138, USA http://dx.doi.org/10.1098/rstb.2018.0248 4Department of Biology, University of Texas Arlington, Arlington, TX 76019, USA 5Department of Biology, and 6Department of Geological Sciences, The University of Texas at Austin, Accepted: 25 February 2019 Austin, MA 78712, USA 7Department of Herpetology, The American Museum of Natural History, New York, NY 10024, USA SL, 0000-0003-4826-0349; DCC, 0000-0002-1629-5726; PG, 0000-0002-3680-2238; One contribution of 16 to a theme issue JFRT, 0000-0002-4730-3805; GAB, 0000-0001-5889-2767; KN, 0000-0002-1088-5282; ‘Convergent evolution in the genomics era: FT-G, 0000-0002-7449-2023; CT, 0000-0002-7013-0762; FB, 0000-0001-6687-8332; new insights and directions’. JAC, 0000-0003-2218-2637; TBS, 0000-0003-1673-9216; SVE, 0000-0003-2535-6217 Evolutionary convergence has been long considered primary evidence of Subject Areas: adaptation driven by natural selection and provides opportunities to explore developmental biology, genomics, evolutionary repeatability and predictability. In recent years, there has been palaeontology, taxonomy and systematics, increased interest in exploring the genetic mechanisms underlying convergent molecular biology evolution, in part, owing to the advent of genomic techniques. However, the current ‘genomics gold rush’ in studies of convergence has overshadowed the reality that most trait classifications are quite broadly defined, resulting Keywords: in incomplete or potentially biased interpretations of results. Genomic studies enhancer, amino acid, bird, eusociality, of convergence would be greatly improved by integrating deep ‘vertical’, natu- pleiotropy, regulatory evolution ral history knowledge with ‘horizontal’ knowledge focusing on the breadth of taxonomic diversity. Natural history collections have and continue to be best positioned for increasing our comprehensive understanding of phenotypic Author for correspondence: diversity, with modern practices of digitization and databasing of morpho- Scott V. Edwards logical traits providing exciting improvements in our ability to evaluate the e-mail: [email protected] degree of morphological convergence. Combining more detailed phenotypic data with the well-established field of genomics will enable scientists to make progress on an important goal in biology: to understand the degree to which genetic or molecular convergence is associated with phenotypic convergence. Although the fields of comparative biology or comparative genomics alone can separately reveal important insights into convergent evolution, here we suggest that the synergistic and complementary roles of natural history collec- tion-derived phenomic data and comparative genomics methods can be particularly powerful in together elucidating the genomic basis of convergent evolution among higher taxa. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’. 1. Introduction Electronic supplementary material is available Convergent evolution is the independent acquisition of similar features in distantly online at https://doi.org/10.6084/m9.figshare. related lineages [1]. Ever since Darwin suggested that similar traits could arise c.4468724. independently in different organisms [2], understanding the underlying causes & 2019 The Author(s) Published by the Royal Society. All rights reserved. 2 natural history royalsocietypublishing.org/journal/rstb morphology ecology behaviour selective forces and developmental constraints functional Phil. Trans. R. Soc. B characterization of genomic convergence phenotypic convergence adaptive/historical 374 scenario : 20180248 genes and regulatory networks locus A locus B gene network Figure 1. Conceptual framework for studies on the genomics of phenotypic convergence. Starting from the top, organismal expertise and knowledge of natural history are the starting points for such studies. Environmental gradients and constraints in physiology, biochemical and developmental pathways may limit or direct trait evolution, potentially driving phenotypic convergence. Phylogenetic comparative methods can be used to test, quantify and visualize instances of convergence. Finally, comparative genomics methods can be used to test whether convergent phenotypes have common underlying genomic mechanisms at various hierarchical levels of individual genetic loci or regulatory networks. Functional validations of genes or pathways identified from genome-wide scans provide means to test the role of specific genomic regions in producing a given convergent phenotype and to attempt a historical reconstruction of evolutionary events. and mechanisms of convergence has been one of the funda- Convergent phenotypes may or may not share a genetic mental objectives of evolutionary biology. Convergent basis at many different hierarchical levels (e.g. nucleotide, evolution has been a central component to study evolutionary gene, protein, regulatory networks, function; figure 1) [5]. predictability [3] by integrating phenotypic, phylogenetic and Additionally, high-levels of pleiotropy, already recognized as environmental data [1,4,5]. While convergent evolution is a likely component of many cases of convergence [17], means usually presumed to be the result of adaptation [6–8], it is that our definition of ‘genomic basis’ of convergence may clear that convergent patterns can also result from non-adaptive require expansion to include the role of individual genes parti- processes such as exaptation, evolutionary constraints, demo- cipating in multiple networks as well as functionally graphic history [1,5,9,10], mutational bias [11] or hemiplasy overlapping networks that may not share many genes. [12,13]. Conceptual differences in defining phenotypic conver- Here, we explore how recent advancements in comparative gence as process-based (when trait similarity evolves by genomics have provided tools to expand genetic studies of con- similar forces of natural selection) versus pattern-based (when vergent phenotypes based on a few candidate genes to entire lineages independently evolve patterns of similar traits, regard- genomes, and how such large-scale genomic data are being less of mechanism) have practical implications for the adequate used to explore the rate and pattern of convergence at different identification and measurement of convergent traits [14]. hierarchical levels. In particular, we highlight the need to In addition to such challenges for defining convergence at the carefully define the convergent phenotype and using the role phenotypic level, additional uncertainties exist for defining of natural history records in aiding this definition. As generat- the genetic basis of phenotypic convergence [15,16]. ing genomic data becomes easier with time, integration of community-wide organismal expertise and natural history character states have proven powerful in guiding comparative 3 collections will remain key to understanding the genomics of genomic analyses [22], finer dissection of convergent pheno- royalsocietypublishing.org/journal/rstb convergence. We focus primarily on convergence among types as a quantitative continuum rather than a binary distantly related species, largely in animals, and generally do phenomenon [34] will allow both an adequate testing of the not discuss convergence among close relatives or populations, adaptive value of the traits in question and a more detailed which are covered elsewhere in this issue [18]. categorization of adaptations themselves. Recent models designed to test the significance of genotype–phenotype associations in a phylogenetic context are an important part 2. Role of organismal expertise in understanding of this new framework [35,36]. An important question is how to derive the most statistical power to detect convergent geno- convergence type–phenotype associations when phenotypes are defined The resurgence of interest in phenotypic convergence is driven continuously or with more than two states. New quantitative by the desire to add a new layer—genomics—to what has been methods of assessing convergence in phenotypic traits a long-standing, centuries-old interest in natural history and [37–39], as well as phylogenetic quantitative genetic models Phil. Trans. R. Soc. B organismal biology (figure 1). Without genomics, studies of [40,41] will both be helpful in accommodating complex phenotypic convergence would no doubt continue as they characters into genomic studies of convergent evolution. have for decades, particularly given the firm foundation of comparative biology on which studies of convergence now (b) Diverse types of natural history knowledge can rest [19,20]. However, the rapidly declining costs of genome sequencing have reinvigorated questions about the