Genomics and the origin of species

Journal name:
Nature Reviews Genetics
Volume:
15,
Pages:
176–192
Year published:
DOI:
doi:10.1038/nrg3644
Published online

Abstract

Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

At a glance

Figures

  1. Genomic patterns of divergence along the 'speciation continuum' of Heliconius spp. butterflies.
    Figure 1: Genomic patterns of divergence along the 'speciation continuum' of Heliconius spp. butterflies.

    The patterns of differentiation between hybridizing parapatric races (part Aa) and sympatric species (part Ac), as well as those between geographically isolated (that is, allopatric) races (part Ab) and species (part Ad), are shown along the genome; the x axes represent chromosome positions. Divergence is highly heterogeneous even between allopatric populations of the same species (part Ab). The shapes of the frequency distributions of locus-specific FST values (part B) clearly differ both between the different stages in the continuum and between geographical scenarios. For example, the greater variance is consistent with gene flow between species in sympatry (part Bc). However, the challenge is to distinguish between speciation with gene flow (parts Ba, Bc) and that without gene flow (parts Bb, Bd). All species shown are from the genus Heliconius, and all subspecies shown are from the species Heliconius melpomene. FG, French Guiana; Pan, Panama; Per, Peru. Figure is modified, with permission, from Ref. 87 © (2013) Cold Spring Harbor Laboratory Press.

  2. Effect sizes of substitutions on phenotype and on reproductive isolation.
    Figure 2: Effect sizes of substitutions on phenotype and on reproductive isolation.

    a | Effects of variation at different levels and the connections between these levels are shown. The size of effect can vary at each step from zero or quite small to very large. A substitution can alter gene expression or protein coding, which in turn has some effect on a phenotype. This phenotype can have effects of varying sizes on environment-dependent fitness and hence possibly extrinsic postzygotic isolation; on environment-independent fitness and hence possibly intrinsic postzygotic isolation; and on prezygotic isolation. Alternatively, a phenotype may pleiotropically affect both fitness and prezygotic isolation. All of these effects combine to generate total reproductive isolation (RI), which will probably increase FST, although other factors also can affect FST. b | There is a lack of correlation between the effect of a locus on phenotype (P) and that on RI, such that phenotypic effect size does not necessarily predict RI effect size. Examples of different relationships between these effect sizes can be found in Bateson–Dobzhansky–Muller incompatibilities (DMIs) in Solanum spp.27, the optix locus in Heliconius spp.159, the cuticular hydrocarbon (CHC) loci in Drosophila spp.200 and the ectodysplasin (EDA) locus in sticklebacks190. The relationships between phenotypic effect size, RI effect size and FST are currently unknown to a large extent.

  3. Influence of genetic constraints on speciation.
    Figure 3: Influence of genetic constraints on speciation.

    a | With the help of next-generation sequencing, it is now feasible to infer relatedness of individuals in any given natural population and thus to estimate a G-matrix without the use of pedigree data172. The G-matrix (represented as an ellipse in the space of two quantitative traits) can bias evolution in certain directions. Depending on the adaptive landscape (represented by regions of higher (+; red) and lower (–; blue) fitness than the parental populations (white and black)), the G-matrix might constrain adaptive divergence and speciation. Hybridization events may facilitate speciation either by aligning the G-matrix in the direction of divergence between parental species (that is, the intermediate hybrid) or by giving rise to novel phenotypes (that is, the transgressive hybrid) in new regions of positive fitness that cannot be reached through gradual evolution in either of the parental species. The influence of genetic constraints on speciation can be tested at the phylogenetic level. b | Constraints may persist over evolutionary time as a result of the inability of divergent selection to change genetic architecture, which prevents speciation from happening. c | Alternatively, other forms of selection (for example, correlational selection) can alter the structure and the orientation of the G-matrix and can potentially facilitate divergence and speciation over moderate timescales. d | Hybridization and gene flow can markedly alter the G-matrix in only a few generations, which 'fuels' adaptive divergence and results in sudden bursts of speciation. Note that hybridization between sister species is shown here for illustration, but hybridization that facilitates divergence may occur more widely among related taxa.

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Author information

Affiliations

  1. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.

    • Ole Seehausen
  2. Department of Animal and Plant Sciences, the University of Sheffield, Sheffield S10 2TN, UK; and the Sven Lovén Centre — Tjärnö, University of Gothenburg, S-452 96 Strömstad, Sweden.

    • Roger K. Butlin
  3. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland; and the Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, 8092 Zürich, Switzerland.

    • Irene Keller
  4. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.

    • Catherine E. Wagner
  5. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and the Department of Zoology; Ecology, Evolutionary Biology and Behavior Program; BEACON Center, Michigan State University, 203 Natural Sciences, East Lansing, Michigan 48824, USA.

    • Janette W. Boughman
  6. Department of Biological Sciences, Institute of Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho 83844–3051, USA.

    • Paul A. Hohenlohe
  7. Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA.

    • Catherine L. Peichel
  8. Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, PO BOX 1066, Blindern, N-0316 Oslo, Norway.

    • Glenn-Peter Saetre
  9. School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.

    • Claudia Bank
  10. Integrated Science Laboratory and the Department of Mathematics and Mathematical Statistics, Umeå University, 90187 Umeå, Sweden.

    • Åke Brännström
  11. Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland.

    • Alan Brelsford
  12. Liverpool School of Tropical Medicine, Liverpool L3 5QA, UK.

    • Chris S. Clarkson
  13. Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, PO BOX 1066, Blindern, N-0316 Oslo, Norway.

    • Fabrice Eroukhmanoff
  14. Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556–0369 USA.

    • Jeffrey L. Feder
  15. Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, 8092 Zürich, Switzerland.

    • Martin C. Fischer
  16. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen, Denmark. Present address: the Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala, Sweden.

    • Andrew D. Foote
  17. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, 78457 Konstanz, Germany.

    • Paolo Franchini
  18. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.

    • Chris D. Jiggins
  19. Friedrich Miescher Laboratory of the Max Planck Society, 72076 Tübingen, Germany.

    • Felicity C. Jones
  20. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057 Zurich, Switzerland.

    • Anna K. Lindholm
  21. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.

    • Kay Lucek
  22. Behavioural Biology Group, Centre for Behaviour and Neurosciences, University of Groningen, PO BOX 11103, 9700 CC Groningen, The Netherlands.

    • Martine E. Maan
  23. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.

    • David A. Marques
  24. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.

    • Simon H. Martin
  25. Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland.

    • Blake Matthews
  26. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.

    • Joana I. Meier
  27. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK; and the Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, 8600 Dübendorf, Switzerland.

    • Markus Möst
  28. Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, California 94720–3160, USA.

    • Michael W. Nachman
  29. Integrated Science Laboratory and Department of Ecology and Environmental Science, Umeå University, 90187 Umeå, Sweden.

    • Etsuko Nonaka
  30. Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.

    • Diana J. Rennison
  31. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland; and Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.

    • Julia Schwarzer
  32. Department of Biology, The University of Texas at Arlington, 76010–0498 Texas, USA.

    • Eric T. Watson
  33. Department of Animal and Plant Sciences, the University of Sheffield, Sheffield S10 2TN, UK.

    • Anja M. Westram
  34. Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, 8092 Zürich, Switzerland.

    • Alex Widmer

Competing interests statement

The authors declare no competing interests.

Corresponding author

Correspondence to:

Author details

  • Ole Seehausen

    Ole Seehausen has studied speciation and hybridization since his Ph.D. at the University of Leiden, the Netherlands, in the 1990s. He is particularly interested in adaptive radiations, such as the cichlid fishes of Lake Victoria and, more recently, the whitefish of pre-alpine European lakes, sticklebacks and trout. He is a professor at the Institute of Ecology and Evolution of the University of Bern, Switzerland, and is the head of a research department at Eawag: Swiss Federal Institute of Aquatic Science and Technology, Lucerne, Switzerland. His laboratory combines ecological and behavioural research with genetics and genomics to investigate processes and mechanisms that are implicated in adaptation, speciation, species coexistence and extinction. Ole Seehausen's homepage.

  • Roger K. Butlin

    Roger K. Butlin has studied speciation since his postdoctoral work with Godfrey Hewitt in the 1980s. He is interested in the processes that generate reproductive isolation and its genetic basis. Reinforcement has been a particular focus of his study. His current projects examine the role of chemosensory genes in aphid host race formation and the genetic basis of parallel local adaptation and speciation in periwinkles. He is a professor of evolutionary biology at the University of Sheffield, UK, and currently holds the 2013 Tage Erlander Guest Professorship at the University of Gothenburg, Sweden.

  • Irene Keller

    Irene Keller is a bioinformatician at the Department of Clinical Research of the University of Bern, Switzerland. She received her Ph.D. from the University of Bern and worked as a postdoctoral fellow with Richard Nichols at Queen Mary University of London, UK, and with Jukka Jokela and Ole Seehausen at Eawag: Swiss Federal Institute of Aquatic Science and Technology, Lucerne, Switzerland, and the University of Bern. Her interests focus on the application of molecular and bioinformatic tools to understand the genetic basis of adaptation, speciation and human disease.

  • Catherine E. Wagner

    Catherine E. Wagner is an evolutionary biologist with interests in speciation and the origins of diversity, as well as the relationships between diversity-generating processes and macroevolutionary patterns. Her research uses population genetic, phylogenetic and comparative methods to study diversification. She is currently a postdoctoral researcher at Eawag: the Swiss Federal Institute of Aquatic Science and Technology, Lucerne, Switzerland, and at the University of Bern, Switzerland, where her work focuses primarily on African cichlid fishes. She obtained her Ph.D. in ecology and evolutionary biology in 2011 from Cornell University, Ithaca, New York, USA.

  • Janette W. Boughman

    Janette W. Boughman and her laboratory study the selective forces that cause speciation in threespine sticklebacks, with a particular focus on sexual selection and its interaction with natural selection to generate reproductive isolation. She uses behavioural experiments in both the laboatory and the field to understand the subtle yet powerful action of these forces on phenotypic and genetic evolution and how this transmits to the genome. She has studied both the accumulation of reproductive isolation and its loss through reverse speciation. Her recent work investigates fitness landscapes at both the phenotypic and genetic level and their role in diversification. She is Associate Professor at Michigan State University, East Lansing, USA.

  • Paul A. Hohenlohe

    Paul A. Hohenlohe is an assistant professor in the Department of Biological Sciences and the Institute for Bioinformatics and Evolutionary Studies at the University of Idaho, Moscow, USA. He obtained his Ph.D. in zoology at the University of Washington, Seattle, USA, in 2000 and subsequently worked as a conservation biologist and postdoctoral researcher. His research focus is on evolutionary genetics and genomics, including the use of restriction-site associated DNA sequencing (RAD-seq) and other tools for studying population genomics and conservation in non-model organisms, experimental evolution and evolutionary quantitative genetics theory.

  • Catherine L. Peichel

    Catherine L. Peichel obtained her Ph.D. in developmental genetics at Princeton University, New Jersey, USA, in 1998. During this time, she became intrigued by the genetic basis of phenotypic differences between species. Thus, during her postdoctoral fellowship with David Kingsley at Stanford University, California, USA, she helped to develop the threespine stickleback as a genetic and genomic model system. She has led a research laboratory since 2003 at the Fred Hutchinson Cancer Research Center in Seattle, Washington, USA. Her laboratory uses various approaches to investigate the genetic and genomic changes that underlie adaptation and speciation in sticklebacks.

  • Glenn-Peter Saetre

    Glenn-Peter Sætre is a professor in evolutionary biology at the University of Oslo, Norway. He obtained his doctorate also in Oslo and worked for several years at Uppsala University, Sweden, as a postdoctoral researcher and assistant professor before returning to Oslo in 2003 as full professor. He studies speciation, hybridization and adaptive evolution, mainly in birds, and combines genomic analysis and population genetics with behavioural and ecological studies. His research laboratory is currently mainly focusing on the genomics of hybrid speciation.

  • Claudia Bank

  • Åke Brännström

  • Alan Brelsford

  • Chris S. Clarkson

  • Fabrice Eroukhmanoff

  • Jeffrey L. Feder

  • Martin C. Fischer

  • Andrew D. Foote

  • Paolo Franchini

  • Chris D. Jiggins

  • Felicity C. Jones

  • Anna K. Lindholm

  • Kay Lucek

  • Martine E. Maan

  • David A. Marques

  • Simon H. Martin

  • Blake Matthews

  • Joana I. Meier

  • Markus Möst

  • Michael W. Nachman

  • Etsuko Nonaka

  • Diana J. Rennison

  • Julia Schwarzer

  • Eric T. Watson

  • Anja M. Westram

  • Alex Widmer

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