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Evolution. 2021 Jun;75(6):1256-1273. doi: 10.1111/evo.14215. Epub 2021 May 05.

Defining the speciation continuum.

Evolution; international journal of organic evolution

Sean Stankowski, Mark Ravinet

Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
  2. Current Address: Sean Stankowski, IST Austria, Klosterneuburg, 3400, Austria.
  3. Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, 0316, Norway.
  4. School of Life Sciences, University of Nottingham, Nottingham, NG7 2RD, United Kingdom.

PMID: 33754340 DOI: 10.1111/evo.14215

Abstract

A primary roadblock to our understanding of speciation is that it usually occurs over a timeframe that is too long to study from start to finish. The idea of a speciation continuum provides something of a solution to this problem; rather than observing the entire process, we can simply reconstruct it from the multitude of speciation events that surround us. But what do we really mean when we talk about the speciation continuum, and can it really help us understand speciation? We explored these questions using a literature review and online survey of speciation researchers. Although most researchers were familiar with the concept and thought it was useful, our survey revealed extensive disagreement about what the speciation continuum actually tells us. This is due partly to the lack of a clear definition. Here, we provide an explicit definition that is compatible with the Biological Species Concept. That is, the speciation continuum is a continuum of reproductive isolation. After outlining the logic of the definition in light of alternatives, we explain why attempts to reconstruct the speciation process from present-day populations will ultimately fail. We then outline how we think the speciation continuum concept can continue to act as a foundation for understanding the continuum of reproductive isolation that surrounds us.

© 2021 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.

Keywords: Comparative analysis; isolating barriers; reproductive isolation; species concepts

References

  1. Aeschbacher, S., J. P. Selby, J. H. Willis, and G. Coop. 2017. Population-genomic inference of the strength and timing of selection against gene flow. Proc. Natl. Acad. Sci. USA 114:7061-7066. - PubMed
  2. Barraclough, T. G. 2019. The evolutionary biology of species. Oxford Univ. Press, Oxford, U.K. - PubMed
  3. Barton, N., and B. O. Bengtsson. 1986. The barrier to genetic exchange between hybridising populations. Heredity 57:357-376. - PubMed
  4. Barton, N. H. 1983. Multilocus clines. Evolution 37:454-471. - PubMed
  5. Barton, N. H. 2000. Genetic hitchhiking. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:1553-1562. - PubMed
  6. Barton, N. H. 2020. On the completion of speciation. Philos. Trans. R. Soc. B Biol. Sci. 375:20190530. - PubMed
  7. Barton, N. H., and M. A. R. De Cara. 2009. The evolution of strong reproductive isolation. Evolution 63:1171-1190. - PubMed
  8. Barton, N. H., and K. S. Gale. 1993. Genetic analysis of hybrid zones. Pp. 13-45 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, U.K. - PubMed
  9. Burri, R., A. Nater, T. Kawakami, C. F. Mugal, P. I. Olason, L. Smeds, A. Suh, L. Dutoit, S. Bureš, L. Z. Garamszegi, et al. 2015. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Res. 25:1656-1665. - PubMed
  10. Butlin, R., A. Debelle, C. Kerth, R. R. Snook, L. W. Beukeboom, R. F. C. Castillo, W. Diao, M. E. Maan, S. Paolucci, F. J. Weissing, et al. 2012. and What do we need to know about speciation? Trends Ecol. Evol. 27:27-39. - PubMed
  11. Butlin, R. K., and S. Stankowski. 2020. Is it time to abandon the biological species concept? No. Natl. Sci. Rev. 7:1400-1401. - PubMed
  12. Butlin, R. K., J. Galindo, and J. W. Grahame. 2008. Sympatric, parapatric or allopatric: the most important way to classify speciation? Philos. Trans. R. Soc. Lond. B Biol. Sci. 363:2997-3007. - PubMed
  13. Cooney, C. R., J. A. Bright, E. J. R. Capp, A. M. Chira, E. C. Hughes, C. J. A. Moody, L. O. Nouri, Z. K. Varley, and G. H. Thomas. 2017. Corrigendum: mega-evolutionary dynamics of the adaptive radiation of birds. Nature 552:430. - PubMed
  14. Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43:362-381. - PubMed
  15. Coyne, J. A., and H. A. Orr 1997. “Patterns of speciation in Drosophila” revisited. Evolution 51:295-303. - PubMed
  16. Coyne, J. A., and H. A. Orr 2004. Speciation. Sinauer Associates, Sunderland, MA. - PubMed
  17. Coughlan, J. M., and D. R. Matute. 2020. The importance of intrinsic postzygotic barriers throughout the speciation process. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375:20190533. - PubMed
  18. Cruickshank, T. E., and M. W. Hahn. 2014. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23:3133-3157. - PubMed
  19. Davey, J. W., S. L. Barker, P. M. Rastas, A. Pinharanda, S. H. Martin, R. Durbin, W. O. McMillan, R. M. Merrill, and C. D. Jiggins. 2017. No evidence for maintenance of a sympatric Heliconius species barrier by chromosomal inversions. Evol. Lett. 1:138-154. - PubMed
  20. Dieckmann, U., M. Doebeli, J. A. Metz, and D. Tautz. 2004. Adaptive speciation. Cambridge Univ. Press, Cambridge, U.K. - PubMed
  21. Drès, M., and J. Mallet. 2002. Host races in plant-feeding insects and their importance in sympatric speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:471-492. - PubMed
  22. Feder, J. L., S. P. Egan, and P. Nosil. 2012. The genomics of speciation-with-gene-flow. Trends Genet. 28:342-350. - PubMed
  23. Flaxman, S. M., J. L. Feder, and P. Nosil. 2013. Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow. Evolution 67:2577-2591. - PubMed
  24. Fraïsse, C., I. Popovic, J. Romiguier, E. Loire, A. Simon, N. Galtier, L. Duret, N. Bierne, X. Vekemans, and C. Roux, 2020. DILS: demographic inferences with linked selection by using ABC. Molecular Ecology Resources. https://doi.org/10.1111/1755-0998.13323. - PubMed
  25. Funk, D. J., P. Nosil, and W. J. Etges. 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. Natl. Acad. Sci. USA 103:3209-3213. - PubMed
  26. Gay, L., P.-A. Crochet, D. A. Bell, and T. Lenormand. 2008. Comparing clines on molecular and phenotypic traits in hybrid zones: a window on tension zone models. Evolution 62:2789-2806. - PubMed
  27. Gould, S. J. 1990. Wonderful life: the burgess shale and the nature of history. WW Norton & Company, New York. - PubMed
  28. Gould, S. J., and M. H. Nitecki. 1988. Evolutionary progress. Univ. of Chicago Press, Chicago. - PubMed
  29. Gourbière, S., and J. Mallet. 2010. Are species real? The shape of the species boundary with exponential failure, reinforcement, and the “missing snowball”. Evolution 64:1-24. - PubMed
  30. Grahame, J. W., C. S. Wilding, and R. K. Butlin. 2006. Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis. Evolution 60:268-278. - PubMed
  31. Harrison, R. G. 2012. The language of speciation. Evolution 66:3643-3657. - PubMed
  32. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Univ. Press, Oxford, U.K. - PubMed
  33. Hendry, A. P. 2009. Ecological speciation! Or the lack thereof? Can. J. Fish. Aquat. Sci. 66:1383-1398. - PubMed
  34. Hendry, A. P., D. I. Bolnick, D. Berner, and C. L. Peichel. 2009. Along the speciation continuum in sticklebacks. J. Fish Biol. 75:2000-2036. - PubMed
  35. Hewitt, G. M. 1988. Hybrid zones-natural laboratories for evolutionary studies. Trends Ecol. Evol. 3:158-167. - PubMed
  36. Hey, J. 2001. The mind of the species problem. Trends Ecol. Evol. 16:326-329. - PubMed
  37. Hudson, R. R. 1990. Gene genealogies and the coalescent process. Pp. 1-42 in D. J. Futuyma and. J. Antonovics, eds. Oxford surveys in evolutionary biology. Vol. 7. Oxford Univ. Press, Oxford, U.K. - PubMed
  38. Irwin, D. E. 2020. Assortative mating in hybrid zones is remarkably ineffective in promoting speciation. Am. Nat. 195:E150-E167. - PubMed
  39. Jiggins, C. D., and J. Mallet. 2000. Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15:250-255. - PubMed
  40. Johnson, E. A., and K. Miyanishi. 2008. Testing the assumptions of chronosequences in succession. Ecol. Lett. 11:419-431. - PubMed
  41. Kelleher, J., Y. Wong, A. W. Wohns, C. Fadil, P. K. Albers, and G. McVean. 2019. Inferring whole-genome histories in large population datasets. Nat. Genet. 51:1330-1338. - PubMed
  42. Kulmuni, J., R. K. Butlin, K. Lucek, V. Savolainen, and A. M. Westram. 2020. Towards the completion of speciation: the evolution of further reproductive isolation once the first barriers are in place. Philos. Trans. R. Soc. B Bio. Sci. 286:20190528. - PubMed
  43. Kimura, M. 1962. On the probability of fixation of mutant genes in a population. Genetics 47:713-719. - PubMed
  44. Kimura, M., and T. Ohta. 1969. The average number of generations until extinction of an individual mutant gene in a finite population. Genetics 63:701-709. - PubMed
  45. Laetsch, D. R., G. Bisschop, S. Aeschbacher, S. H. Martin, D. Setter, and K. Lohse. Demographically explicit scans for barriers to gene flow using genome-wide IM blockwise likelihood estimation: gIMble. Unpublished manuscript. - PubMed
  46. Lohse, K., M. Clarke, M. G. Ritchie, and W. J. Etges. 2015. Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation. Evolution 69:1178-1190. - PubMed
  47. Lohse, K., M. Chmelik, S. H. Martin, and N. H. Barton. 2016. Efficient strategies for calculating blockwise likelihoods under the coalescent. Genetics 202:775-786. - PubMed
  48. Lowry, D. B. 2012. Ecotypes and the controversy over stages in the formation of new species. Biol. J. Linn. Soc. Lond. 106:241-257. - PubMed
  49. Lowry, D. B., and B. A. Gould. 2016. Speciation continuum. Elsevier, Amsterdam, The Netherlands. - PubMed
  50. Lyell, C. 1830. Principles of geology. Vol. 1. Univ. of Chicago Press, Chicago. - PubMed
  51. Mallet. 2009. Alfred Russel Wallace and the Darwinian Species Concept: His Paper on the Swallowtail Butterflies (Papilionidae) of 1865. Gayana 73: 42-54 - PubMed
  52. Marques, D. A., K. Lucek, J. I. Meier, S. Mwaiko, C. E. Wagner, L. Excoffier, and O. Seehausen. 2016. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLoS Genet. 12:e1005887. - PubMed
  53. Martin, Simon H., Kanchon K. Dasmahapatra, Nicola J. Nadeau, Camilo Salazar, James R. Walters, Fraser Simpson, Mark Blaxter, Andrea Manica, James Mallet, and Chris D. Jiggins. 2013. “Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research 23:1817-1828. - PubMed
  54. Martin, S. H., J. W. Davey, and C. D. Jiggins. 2015. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Mol. Biol. Evol. 32:244-257. - PubMed
  55. Matute, D. R., and B. S. Cooper. 2021. Comparative studies on speciation: 30 years since Coyne and Orr. Evolution. https://doi.org/10.1111/evo.14181. - PubMed
  56. Mayr, E. 1942. Systematics and the origin of species from the viewpoint of a zoologist. Columbia University Press, New York. - PubMed
  57. Merot, C., C. Salazar, R. M. Merrill, C. D. Jiggins, and M. Joron. 2017. What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies. Proc. R. Soc. B Biol. Sci. 284:20170335. - PubMed
  58. Merrill, R. M., Z. Gompert, L. M. Dembeck, M. R. Kronforst, W. O. McMillan, and C. D. Jiggins. 2011. Mate preference across the speciation continuum in a clade of mimetic butterflies. Evolution 65:1489-1500. - PubMed
  59. Moyle, L. C., and T. Nakazato. 2010. Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521-1523. - PubMed
  60. Moyle, L. C., M. S. Olson, and P. Tiffin. 2004. Patterns of reproductive isolation in three angiosperm genera. Evolution 58:1195-1208. - PubMed
  61. Nordborg, M., and P. Donnelly. 1997. The coalescent process with selfing. Genetics 146:1185-1195. - PubMed
  62. Nosil, P. 2012. Ecological speciation. Oxford Univ. Press, Oxford, U.K. - PubMed
  63. Nosil, P. 2013. Degree of sympatry affects reinforcement in Drosophila. Evolution 67:868-872. - PubMed
  64. Nosil, P., and J. L. Feder. 2012. Genomic divergence during speciation: causes and consequences. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 367: 332-342. - PubMed
  65. Nosil, P., L. J. Harmon, and O. Seehausen. 2009. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24:145-156. - PubMed
  66. Orr, H. A., and M. Turelli. 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55:1085-1094. - PubMed
  67. Patterson, N., P. Moorjani, Y. Luo, S. Mallick, N. Rohland, Y. Zhan, T. Genschoreck, T. Webster, and D. Reich. 2012. Ancient admixture in human history. Genetics 192:1065-1093. - PubMed
  68. Perini, S., M. Rafajlović, A. M. Westram, K. Johannesson, and R. K. Butlin. 2020. Assortative mating, sexual selection, and their consequences for gene flow in Littorina. Evolution 74: 1482-1497. - PubMed
  69. Phadnis, N., E. P. Baker, J. C. Cooper, K. A. Frizzell, E. Hsieh, A. F. A. de la Cruz, J. Shendure, J. O. Kitzman, and H. S. Malik. 2015. An essential cell cycle regulation gene causes hybrid inviability in Drosophila. Science 350:1552-1555. - PubMed
  70. Phillips, B. L., S. J. E. Baird, and C. Moritz. 2004. When vicars meet: a narrow contact zone between morphologically cryptic phylogeographic lineages of the rainforest skink, Carlia rubrigularis. Evolution 58:1536-1548. - PubMed
  71. Phillips, J. D. 2015. The robustness of chronosequences. Ecol. Modell. 298:16-23. - PubMed
  72. Presgraves, D. C. 2002. Patterns of postzygotic isolation in Lepidoptera. Evolution 56:1168-1183. - PubMed
  73. Price, T. D., and M. M. Bouvier. 2002. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083-2089. - PubMed
  74. Rabosky, D. L., F. Santini, J. Eastman, S. A. Smith, B. Sidlauskas, J. Chang, and M. E. Alfaro. 2013. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat. Commun. 4:1958. - PubMed
  75. Räsänen, K., and A. P. Hendry. 2008. Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecol. Lett. 11:624-636. - PubMed
  76. Ravinet, M., R. Faria, R. K. Butlin, J. Galindo, N. Bierne, M. Rafajlović, M. A. F. Noor, B. Mehlig, and A. M. Westram. 2017. Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. J. Evol. Biol. 30:1450-1477. - PubMed
  77. Ravinet, M., K. Yoshida, S. Shigenobu, A. Toyoda, A. Fujiyama, and J. Kitano. 2018. The genomic landscape at a late stage of stickleback speciation: high genomic divergence interspersed by small localized regions of introgression. PLoS Genet. 14:e1007358. - PubMed
  78. Richards, R. A. 2010. The species problem: a philosophical analysis. Cambridge Univ. Press, Cambridge, U.K. - PubMed
  79. Ringbauer, H., A. Kolesnikov, D. L. Field, and N. H. Barton. 2018. Estimating barriers to gene flow from distorted isolation-by-distance patterns. Genetics 208:1231-1245. - PubMed
  80. Roesti, M., S. Gavrilets, A. P. Hendry, W. Salzburger, and D. Berner. 2014. The genomic signature of parallel adaptation from shared genetic variation. Molecular Ecology, 23: 3944-3956. - PubMed
  81. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219-1228. - PubMed
  82. Roux, C., C. Fraïsse, J. Romiguier, Y. Anciaux, N. Galtier, and N. Bierne. 2016. Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biol. 14:e2000234. - PubMed
  83. Russell, S. T. 2003. Evolution of intrinsic post-zygotic reproductive isolation in fish. Ann. Zool. Fennici 40:321-329. - PubMed
  84. Seehausen, O. 2009. Progressive levels of trait divergence along a ‘speciation transect’ in the Lake Victoria cichlid fish Pundamilia. Pp. 155-176 in R. K. Butlin, J. R. Bridle, and D. Schluter, eds. Speciation and patterns of diversity. Cambridge Univ. Press, Cambridge, U.K. - PubMed
  85. Seehausen, O., R. K. Butlin, I. Keller, C. E. Wagner, J. W. Boughman, P. A. Hohenlohe, C. L. Peichel, G.-P. Saetre, C. Bank, A. Brännström, et al. 2014. Genomics and the origin of species. Nat. Rev. Genet. 15:176-192. - PubMed
  86. Servedio, M. R., and J. Hermisson. 2019. The evolution of partial reproductive isolation as an adaptive optimum. Evolution 74:4-14. - PubMed
  87. Shaw, K. L., and S. P. Mullen. 2014. Speciation continuum. J. Hered. 105:741-742. - PubMed
  88. Smadja, C. M., and R. K. Butlin. 2011. A framework for comparing processes of speciation in the presence of gene flow. Mol. Ecol. 20:5123-5140. - PubMed
  89. Sobel, J. M. 2014. Ecogeographic isolation and speciation in the genus Mimulus. Am. Nat. 184:565-579. - PubMed
  90. Sobel, J. M., and G. F. Chen. 2014. Unification of methods for estimating the strength of reproductive isolation. Evolution 68:1511-1522. - PubMed
  91. Sobel, J. M., G. F. Chen, L. R. Watt, and D. W. Schemske. 2010. The biology of speciation. Evolution 64:295-315. - PubMed
  92. Stelkens, R. B., K. A. Young, and O. Seehausen. 2010. The accumulation of reproductive incompatibilities in African cichlid fish. Evolution 64:617-633. - PubMed
  93. Stelkens, R. B., C. Schmid, and O. Seehausen. 2015. Hybrid breakdown in cichlid fish. PLoS One 10:e0127207. - PubMed
  94. Stankowski, S., M. A. Chase, A. M. Fuiten, M. F. Rodrigues, P. L. Ralph, and M. A. Streisfeld. 2019. Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers. PLoS Biol. 17:e3000391. - PubMed
  95. Stankowski, S., and M. Ravinet. In Press. Quantifying the use of species concepts. Current Biology. - PubMed
  96. Supple, M. A., R. Papa, H. M. Hines, W. O. McMillan, and B. A. Counterman. 2015. Divergence with gene flow across a speciation continuum of Heliconius butterflies. BMC Evolutionary Biology. 15: 1-12. - PubMed
  97. Tajima, F. 1989. The effect of change in population size on DNA polymorphism. Genetics 123:597-601. - PubMed
  98. Taylor, E. B., J. W. Boughman, M. Groenenboom, M. Sniatynski, D. Schluter, and J. L. Gow. 2006. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology. 15: 343-355. - PubMed
  99. Turelli, M., J. R. Lipkowitz, J. R., and Y. Brandvain. 2014. On the Coyne and Orr-igin of species: effects of intrinsic postzygotic isolation, ecological differentiation, X chromosome size, and sympatry on Drosophila speciation. Evolution 68:1176-1187. - PubMed
  100. Turner, T. L., M. W. Hahn, and S. V. Nuzhdin. 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3:e285. - PubMed
  101. Walker, L. R., D. A. Wardle, R. D. Bardgett, and B. D. Clarkson. 2010. The use of chronosequences in studies of ecological succession and soil development. J. Ecol. 98:725-736. - PubMed
  102. Wallace, A. R. 1865. I. On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Trans. Linn. Soc. Lond. 25:1-71. - PubMed
  103. Walsh, B. D. 1864. On phytophagic varieties and phytophagous species. Proc. Entomol. Soc. Phila. 3:403-430. - PubMed
  104. White, N. J., R. R. Snook, and I. Eyres. 2020. The past and future of experimental speciation. Trends Ecol. Evol. 35:10-21. - PubMed
  105. Whitlock, M. C., and D. E. Mccauley. 1999. Indirect measures of gene flow and migration: FST ≠ 1/(4Nm+1). Heredity 82:117-125. - PubMed
  106. Wright, S. 1943. Isolation by distance. Genetics 28:114-138. - PubMed
  107. Wu, C.-I. 2001. The genic view of the process of speciation. J. Evol. Biol. 14:851-865. - PubMed
  108. Wu, C. I., and C. T. Ting. 2004. Genes and speciation. Nature Reviews Genetics. 5: 114-122. - PubMed
  109. Yukilevich, R. 2012. Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila. Evolution 66:1430-1446. - PubMed

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