1932

Abstract

Evolutionary radiations are responsible for much of the variation in biodiversity across taxa. Cichlid fishes are well known for spectacular evolutionary radiations, as they have repeatedly evolved into large and phenotypically diverse arrays of species. Cichlid genomes carry signatures of past events and, at the same time, are the substrate for ongoing evolution. We survey genome-wide data and the available literature covering 438 cichlid populations (412 species) across multiple radiations to synthesize information about patterns and sharing of genetic variation. Nucleotide diversity within species is low in cichlids, with 92% of surveyed populations having less diversity than the median value found in other vertebrates. Divergence within radiations is also low, and a large proportion of variation is shared among species due to incomplete lineage sorting and widespread hybridization. Population genetics therefore provides a suitable conceptual framework for evolutionary genomic studies of cichlid radiations. We focus in detail on the roles of hybridization in shaping the patterns of genetic variation and in promoting cichlid diversification.

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2021-02-15
2024-10-12
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Literature Cited

  1. 1. 
    Aristotle. 1965. History of Animals, Vol. I: Books 1–3 Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  2. 2. 
    Barton NH. 2007. Evolution Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
    [Google Scholar]
  3. 3. 
    Charlesworth B, Charlesworth D. 2010. Elements of Evolutionary Genetics Greenwood Village, CO: Roberts & Co.
    [Google Scholar]
  4. 4. 
    Zerbino DR, Paten B, Haussler D 2012. Integrating genomes. Science 336:6078179–82
    [Google Scholar]
  5. 5. 
    Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW et al. 2014. Genomics and the origin of species. Nat. Rev. Genet. 15:3176–92
    [Google Scholar]
  6. 6. 
    Berner D, Salzburger W. 2015. The genomics of organismal diversification illuminated by adaptive radiations. Trends Genet 31:9491–99
    [Google Scholar]
  7. 7. 
    Koepfli K-P, Paten B 2015. The Genome 10K Project: a way forward. Annu. Rev. Anim. Biosci. 3:57–111
    [Google Scholar]
  8. 8. 
    Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J et al. 2018. Earth BioGenome Project: sequencing life for the future of life. PNAS 115:174325–33
    [Google Scholar]
  9. 9. 
    Taylor SA, Larson EL. 2019. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3:2170–77
    [Google Scholar]
  10. 10. 
    Kocher TD. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 5:4288–98
    [Google Scholar]
  11. 11. 
    Seehausen O. 2007. Evolution and ecological theory: Chance, historical contingency and ecological determinism jointly determine the rate of adaptive radiation. Heredity 99:361–63
    [Google Scholar]
  12. 12. 
    Turner GF. 2007. Adaptive radiation of cichlid fish. Curr. Biol. 17:19R827–31
    [Google Scholar]
  13. 13. 
    Santos ME, Salzburger W. 2012. Evolution. How cichlids diversify. Science 338:6107619–21
    [Google Scholar]
  14. 14. 
    Seehausen O. 2015. Process and pattern in cichlid radiations—inferences for understanding unusually high rates of evolutionary diversification. New Phytol 207:2304–12
    [Google Scholar]
  15. 15. 
    Salzburger W. 2018. Understanding explosive diversification through cichlid fish genomics. Nat. Rev. Genet. 19:11705–17
    [Google Scholar]
  16. 16. 
    Leinonen R, Sugawara H 2011. The sequence read archive. Nucleic Acids Res 39:Database IssueD19–D21
    [Google Scholar]
  17. 17. 
    Meier JI, Marques DA, Mwaiko S, Wagner CE, Excoffier L, Seehausen O 2017. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8:14363
    [Google Scholar]
  18. 18. 
    Meier JI, Stelkens RB, Joyce DA, Mwaiko S, Phiri N et al. 2019. The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlid fishes. Nat. Commun. 10:5391
    [Google Scholar]
  19. 19. 
    Willis SC, Macrander J, Farias IP, Ortí G 2012. Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data. BMC Evol. Biol. 12:96
    [Google Scholar]
  20. 20. 
    Malinsky M, Svardal H, Tyers AM, Miska EA, Genner MJ et al. 2018. Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nat. Ecol. Evol. 2:121940–55
    [Google Scholar]
  21. 21. 
    Meyer BS, Matschiner M, Salzburger W 2016. Disentangling incomplete lineage sorting and introgression to refine species-tree estimates for Lake Tanganyika cichlid fishes. Syst. Biol. 66:4531–50
    [Google Scholar]
  22. 22. 
    Gante HF, Matschiner M, Malmstrøm M, Jakobsen KS, Jentoft S, Salzburger W 2016. Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika. Mol. Ecol. 25:246143–61
    [Google Scholar]
  23. 23. 
    Irisarri I, Singh P, Koblmüller S, Torres-Dowdall J, Henning F et al. 2018. Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes. Nat. Commun. 9:3159
    [Google Scholar]
  24. 24. 
    Wiens JJ. 2017. What explains patterns of biodiversity across the Tree of Life. BioEssays 39:31600128
    [Google Scholar]
  25. 25. 
    Matschiner M. 2019. Gondwanan vicariance or trans-Atlantic dispersal of cichlid fishes: a review of the molecular evidence. Hydrobiologia 832:9–37
    [Google Scholar]
  26. 26. 
    Ronco F, Matschiner M, Böhne A, Boila A, Büscher H et al. 2020. Drivers and dynamics of a massive adaptive radiation in African cichlid fishes. Nature In press
    [Google Scholar]
  27. 27. 
    Matschiner M, Böhne A, Ronco F, Salzburger W 2020. The genomic timeline of cichlid fish diversification across continents. Nat. Commun. 11:15895
    [Google Scholar]
  28. 28. 
    Barlow G. 2008. The Cichlid Fishes: Nature's Grand Experiment in Evolution New York: Basic Books
    [Google Scholar]
  29. 29. 
    Salzburger W. 2009. The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol. Ecol. 18:2169–85
    [Google Scholar]
  30. 30. 
    Salzburger W, Van Bocxlaer B, Cohen AS 2014. Ecology and evolution of the African Great Lakes and their faunas. Annu. Rev. Ecol. Evol. Syst. 45:519–45
    [Google Scholar]
  31. 31. 
    Fryer G, Iles TD. 1972. The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution Edinburgh, UK: Oliver & Boyd
    [Google Scholar]
  32. 32. 
    Brawand D, Wagner CE, Li YI, Malinsky M, Keller I et al. 2014. The genomic substrate for adaptive radiation in African cichlid fish. Nature 513:375–81
    [Google Scholar]
  33. 33. 
    Ivory SJ, Blome MW, King JW, McGlue MM, Cole JE, Cohen AS 2016. Environmental change explains cichlid adaptive radiation at Lake Malawi over the past 1.2 million years. PNAS 113:4211895–900
    [Google Scholar]
  34. 34. 
    Malinsky M, Salzburger W. 2016. Environmental context for understanding the iconic adaptive radiation of cichlid fishes in Lake Malawi. PNAS 113:4211654–56
    [Google Scholar]
  35. 35. 
    Verheyen E. 2003. Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300:5617325–29
    [Google Scholar]
  36. 36. 
    Kocher TD, Conroy JA, McKaye KR, Stauffer JR 1993. Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. Mol. Phylogenet. Evol. 2:2158–65
    [Google Scholar]
  37. 37. 
    Muschick M, Indermaur A, Salzburger W 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Curr. Biol. 22:242362–68
    [Google Scholar]
  38. 38. 
    Ronco F, Büscher HH, Indermaur A, Salzburger W 2019. The taxonomic diversity of the cichlid fish fauna of ancient Lake Tanganyika, East Africa. J. Great Lakes Res. 46:1067–78
    [Google Scholar]
  39. 39. 
    Konings A. 2007. Malaŵi Cichlids in Their Natural Habitat El Paso, TX: Cichlid. , 4th ed..
    [Google Scholar]
  40. 40. 
    Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL 2001. How many species of cichlid fishes are there in African lakes. Mol. Ecol. 10:3793–806
    [Google Scholar]
  41. 41. 
    Wagner CE, Harmon LJ, Seehausen O 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487:7407366–69
    [Google Scholar]
  42. 42. 
    Fan S, Elmer KR, Meyer A 2012. Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages. Philos. Trans. R. Soc. B Biol. Sci. 367:1587385–94
    [Google Scholar]
  43. 43. 
    Musilová Z, Indermaur A, Bitja‐Nyom AR, Omelchenko D, Kłodawska M et al. 2019. Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon. Mol. Ecol. 28:235010–31
    [Google Scholar]
  44. 44. 
    Malinsky M, Challis RJ, Tyers AM, Schiffels S, Terai Y et al. 2015. Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. Science 350:62671493–98
    [Google Scholar]
  45. 45. 
    Moser FN, van Rijssel JC, Mwaiko S, Meier JI, Ngatunga B, Seehausen O 2018. The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes. Proc. R. Soc. B Biol. Sci. 285:188420180171
    [Google Scholar]
  46. 46. 
    Coyne JA, Orr HA. 2004. Speciation Sunderland, MA: Sinauer Assoc.
    [Google Scholar]
  47. 47. 
    Barluenga M, Stölting KN, Salzburger W, Muschick M, Meyer A 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:7077719–23
    [Google Scholar]
  48. 48. 
    Elmer KR, Fan S, Kusche H, Spreitzer ML, Kautt AF et al. 2014. Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes. Nat. Commun. 5:5168
    [Google Scholar]
  49. 49. 
    Kautt AF, Machado-Schiaffino G, Meyer A 2016. Multispecies outcomes of sympatric speciation after admixture with the source population in two radiations of Nicaraguan Crater Lake cichlids. PLOS Genet 12:6e1006157
    [Google Scholar]
  50. 50. 
    López-Fernández H, Arbour JH, Winemiller KO, Honeycutt RL 2013. Testing for ancient adaptive radiations in Neotropical cichlid fishes. Evolution 67:51321–37
    [Google Scholar]
  51. 51. 
    Schwarzer J, Misof B, Ifuta SN, Schliewen UK 2011. Time and origin of cichlid colonization of the lower Congo rapids. PLOS ONE 6:7e22380
    [Google Scholar]
  52. 52. 
    Burress ED, Piálek L, Casciotta JR, Almirón A, Tan M et al. 2018. Island- and lake-like parallel adaptive radiations replicated in rivers. Proc. R. Soc. B Biol. Sci. 285:187020171762
    [Google Scholar]
  53. 53. 
    Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15:81034–50
    [Google Scholar]
  54. 54. 
    Lander ES. 2011. Initial impact of the sequencing of the human genome. Nature 470:7333187–97
    [Google Scholar]
  55. 55. 
    Loh Y-HE, Bezault E, Muenzel FM, Roberts RB, Swofford R et al. 2013. Origins of shared genetic variation in African cichlids. Mol. Biol. Evol. 30:4906–17
    [Google Scholar]
  56. 56. 
    Sudmant PH, Rausch T, Gardner EJ, Handsaker RE, Abyzov A et al. 2015. An integrated map of structural variation in 2,504 human genomes. Nature 526:757175–81
    [Google Scholar]
  57. 57. 
    Mérot C, Oomen RA, Tigano A, Wellenreuther M 2020. A roadmap for understanding the evolutionary significance of structural genomic variation. Trends Ecol. Evol. 35:7561–72
    [Google Scholar]
  58. 58. 
    Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V et al. 2014. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515:7526261–63
    [Google Scholar]
  59. 59. 
    Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L et al. 2012. Revisiting an old riddle: What determines genetic diversity levels within species. PLOS Biol 10:9e1001388
    [Google Scholar]
  60. 60. 
    Ellegren H, Galtier N. 2016. Determinants of genetic diversity. Nat. Rev. Genet. 17:7422–33
    [Google Scholar]
  61. 61. 
    Barton NH, Keightley PD. 2002. Understanding quantitative genetic variation. Nat. Rev. Genet. 3:11–21
    [Google Scholar]
  62. 62. 
    Barrett RDH, Schluter D. 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:138–44
    [Google Scholar]
  63. 63. 
    Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:739255–61
    [Google Scholar]
  64. 64. 
    Abascal F, Corvelo A, Cruz F, Villanueva-Cañas JL, Vlasova A et al. 2016. Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx. Genome Biol 17:251
    [Google Scholar]
  65. 65. 
    Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M et al. 2015. Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature 518:7539371–75
    [Google Scholar]
  66. 66. 
    Bourgeois Y, Ruggiero RP, Manthey JD, Boissinot S 2019. Recent secondary contacts, linked selection, and variable recombination rates shape genomic diversity in the model species Anolis carolinensis. Genome Biol. Evol 11:72009–22
    [Google Scholar]
  67. 67. 
    Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10:3195–205
    [Google Scholar]
  68. 68. 
    Naciri Y, Linder HP. 2020. The genetics of evolutionary radiations. Biol. Rev. 95:1055–72
    [Google Scholar]
  69. 69. 
    Kautt AF, Machado-Schiaffino G, Meyer A 2018. Lessons from a natural experiment: allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way. Evol. Lett. 2:4323–40
    [Google Scholar]
  70. 70. 
    Schiffels S, Durbin R. 2014. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46:8919–25
    [Google Scholar]
  71. 71. 
    Speidel L, Forest M, Shi S, Myers SR 2019. A method for genome-wide genealogy estimation for thousands of samples. Nat. Genet. 51:91321–29
    [Google Scholar]
  72. 72. 
    Ford AGP, Dasmahapatra KK, Rüber L, Gharbi K, Cezard T, Day JJ 2015. High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment. Mol. Ecol. 24:133421–40
    [Google Scholar]
  73. 73. 
    McGee MD, Neches RY, Seehausen O 2016. Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Mol. Ecol. 25:1260–68
    [Google Scholar]
  74. 74. 
    Svardal H, Quah FX, Malinsky M, Ngatunga BP, Miska EA et al. 2020. Ancestral hybridization facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation. Mol. Biol. Evol. 37:41100–13
    [Google Scholar]
  75. 75. 
    Carleton KL, Conte M, Malinsky M, Nandamuri SP, Sandkam BA et al. 2020. Movement of transposable elements contributes to cichlid diversity. Mol. Ecol. 2949
    [Google Scholar]
  76. 76. 
    Alter SE, Munshi-South J, Stiassny MLJ 2017. Genomewide SNP data reveal cryptic phylogeographic structure and microallopatric divergence in a rapids-adapted clade of cichlids from the Congo River. Mol. Ecol. 26:51401–19
    [Google Scholar]
  77. 77. 
    Carvajal-Vallejos FM, Duponchelle F, Ballivian JPT, Hubert N, Rodríguez JN et al. 2010. Population genetic structure of Cichla pleiozona (Perciformes: Cichlidae) in the Upper Madera basin (Bolivian Amazon): Sex-biased dispersal. Mol. Phylogenet. Evol. 57:31334–40
    [Google Scholar]
  78. 78. 
    Lewontin RC. 1974. The Genetic Basis of Evolutionary Change New York: Columbia Univ. Press
    [Google Scholar]
  79. 79. 
    Guerrero RF, Hahn MW. 2017. Speciation as a sieve for ancestral polymorphism. Mol. Ecol. 26:205362–68
    [Google Scholar]
  80. 80. 
    Paul JS, Albrechtsen A, Song YS 2011. Genotype and SNP calling from next-generation sequencing data. Nat. Rev. Genet. 12:6443–51
    [Google Scholar]
  81. 81. 
    Lunter G, Goodson M. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21:6936–39
    [Google Scholar]
  82. 82. 
    Moran P, Kornfield I. 1993. Retention of an ancestral polymorphism in the mbuna species flock (Teleostei: Cichlidae) of Lake Malawi. Mol. Biol. Evol. 10:51015–29
    [Google Scholar]
  83. 83. 
    Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I et al. 2012. Insights into hominid evolution from the gorilla genome sequence. Nature 483:7388169–75
    [Google Scholar]
  84. 84. 
    Meier JI, Marques DA, Wagner CE, Excoffier L, Seehausen O 2018. Genomics of parallel ecological speciation in Lake Victoria cichlids. Mol. Biol. Evol. 35:61489–506
    [Google Scholar]
  85. 85. 
    Fijarczyk A, Babik W. 2015. Detecting balancing selection in genomes: limits and prospects. Mol. Ecol. 24:143529–45
    [Google Scholar]
  86. 86. 
    Savolainen O, Lascoux M, Merilä J 2013. Ecological genomics of local adaptation. Nat. Rev. Genet. 14:11807–20
    [Google Scholar]
  87. 87. 
    Svardal H, Rueffler C, Hermisson J 2015. A general condition for adaptive genetic polymorphism in temporally and spatially heterogeneous environments. Theor. Popul. Biol. 99:76–97
    [Google Scholar]
  88. 88. 
    Carvalho CMB, Lupski JR. 2016. Mechanisms underlying structural variant formation in genomic disorders. Nat. Rev. Genet. 17:4224–38
    [Google Scholar]
  89. 89. 
    Brookfield JFY. 2005. The ecology of the genome—mobile DNA elements and their hosts. Nat. Rev. Genet. 6:2128–36
    [Google Scholar]
  90. 90. 
    Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9:5397–405
    [Google Scholar]
  91. 91. 
    Fan S, Meyer A. 2014. Evolution of genomic structural variation and genomic architecture in the adaptive radiations of African cichlid fishes. Front. Genet. 5:163
    [Google Scholar]
  92. 92. 
    Simonti CN, Pavlicev M, Capra JA 2017. Transposable element exaptation into regulatory regions is rare, influenced by evolutionary age, and subject to pleiotropic constraints. Mol. Biol. Evol. 34:112856–69
    [Google Scholar]
  93. 93. 
    Zeng L, Pederson SM, Kortschak RD, Adelson DL 2018. Transposable elements and gene expression during the evolution of amniotes. Mob. DNA 9:17
    [Google Scholar]
  94. 94. 
    Santos ME, Braasch I, Boileau N, Meyer BS, Sauteur L et al. 2014. The evolution of cichlid fish egg-spots is linked with a cis-regulatory change. Nat. Commun. 5:5149
    [Google Scholar]
  95. 95. 
    Conte MA, Gammerdinger WJ, Bartie KL, Penman DJ, Kocher TD 2017. A high quality assembly of the Nile tilapia (Oreochromis niloticus) genome reveals the structure of two sex determination regions. BMC Genom 18:341
    [Google Scholar]
  96. 96. 
    Conte MA, Joshi R, Moore EC, Nandamuri SP, Gammerdinger WJ et al. 2019. Chromosome-scale assemblies reveal the structural evolution of African cichlid genomes. GigaScience 8:4giz030
    [Google Scholar]
  97. 97. 
    Ferreira IA, Poletto AB, Kocher TD, Mota-Velasco JC, Penman DJ, Martins C 2010. Chromosome evolution in African cichlid fish: contributions from the physical mapping of repeated DNAs. Cytogenet. Genome Res. 129:4314–22
    [Google Scholar]
  98. 98. 
    Clark FE, Conte MA, Ferreira-Bravo IA, Poletto AB, Martins C, Kocher TD 2017. Dynamic sequence evolution of a sex-associated B chromosome in Lake Malawi cichlid fish. J. Hered. 108:153–62
    [Google Scholar]
  99. 99. 
    Ozouf-Costaz C, Coutanceau JP, Bonillo C, Mercot H, Fermon Y, Guidi-Rotani C 2017. New insights into the chromosomal differentiation patterns among cichlids from Africa and Madagascar. Cybium 41:135–43
    [Google Scholar]
  100. 100. 
    Poletto AB, Ferreira IA, Cabral-de-Mello DC, Nakajima RT, Mazzuchelli J et al. 2010. Chromosome differentiation patterns during cichlid fish evolution. BMC Genet 11:50
    [Google Scholar]
  101. 101. 
    Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H et al. 2011. B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLOS Genet 7:8e1002203
    [Google Scholar]
  102. 102. 
    Gross MC, Feldberg E, Cella DM, Schneider MC, Schneider CH et al. 2009. Intriguing evidence of translocations in Discus fish (Symphysodon, Cichlidae) and a report of the largest meiotic chromosomal chain observed in vertebrates. Heredity 102:5435–41
    [Google Scholar]
  103. 103. 
    Rhie A, McCarthy SA, Fedrigo O, Damas J, Formenti G et al. 2020. Towards complete and error-free genome assemblies of all vertebrate species. bioRxiv. https://doi.org/10.1101/2020.05.22.110833
    [Crossref] [Google Scholar]
  104. 104. 
    Mallet J, Besansky N, Hahn MW 2016. How reticulated are species. BioEssays 38:2140–49
    [Google Scholar]
  105. 105. 
    Novikova PY, Hohmann N, Nizhynska V, Tsuchimatsu T, Ali J et al. 2016. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat. Genet. 48:91077–82
    [Google Scholar]
  106. 106. 
    Svardal H, Jasinska AJ, Apetrei C, Coppola G, Huang Y et al. 2017. Ancient hybridization and strong adaptation to viruses across African vervet monkey populations. Nat. Genet. 49:121705–13
    [Google Scholar]
  107. 107. 
    Stryjewski KF, Sorenson MD. 2017. Mosaic genome evolution in a recent and rapid avian radiation. Nat. Ecol. Evol. 1:121912–22
    [Google Scholar]
  108. 108. 
    Edelman NB, Frandsen PB, Miyagi M, Clavijo B, Davey J et al. 2019. Genomic architecture and introgression shape a butterfly radiation. Science 366:6465594–99
    [Google Scholar]
  109. 109. 
    Seehausen O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol. 19:4198–207
    [Google Scholar]
  110. 110. 
    Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE et al. 2013. Hybridization and speciation. J. Evol. Biol. 26:2229–46
    [Google Scholar]
  111. 111. 
    Schumer M, Rosenthal GG, Andolfatto P 2014. How common is homoploid hybrid speciation?. 6861553–60
  112. 112. 
    Lamichhaney S. 2018. Rapid hybrid speciation in Darwin's finches. Science 359:6372224–28
    [Google Scholar]
  113. 113. 
    Marques DA, Meier JI, Seehausen O 2019. A combinatorial view on speciation and adaptive radiation. Trends Ecol. Evol. 34:6531–44
    [Google Scholar]
  114. 114. 
    Stelkens RB, Schmid C, Seehausen O 2015. Hybrid breakdown in cichlid fish. PLOS ONE 10:5e0127207
    [Google Scholar]
  115. 115. 
    Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV et al. 2011. Comparative and demographic analysis of orang-utan genomes. Nature 469:7331529–33
    [Google Scholar]
  116. 116. 
    Franchini P, Fruciano C, Spreitzer ML, Jones JC, Elmer KR et al. 2014. Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes. Mol. Ecol. 23:71828–45
    [Google Scholar]
  117. 117. 
    Nico LG, Beamish WH, Musikasinthorn P 2007. Discovery of the invasive Mayan Cichlid fish “Cichlasomaurophthalmus (Günther 1862) in Thailand, with comments on other introductions and potential impacts. Aquat. Invas. 2:3197–214
    [Google Scholar]
  118. 118. 
    Keller I, Wagner CE, Greuter L, Mwaiko S, Selz OM et al. 2013. Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Mol. Ecol. 22:112848–63
    [Google Scholar]
  119. 119. 
    Meier JI, Sousa VC, Marques DA, Selz OM, Wagner CE et al. 2017. Demographic modelling with whole‐genome data reveals parallel origin of similar Pundamilia cichlid species after hybridization. Mol. Ecol. 26:1123–41
    [Google Scholar]
  120. 120. 
    Olave M, Meyer A 2020. Implementing large genomic single nucleotide polymorphism data sets in phylogenetic network reconstructions: a case study of particularly rapid radiations of cichlid fish. Syst. Biol. 69:5848–62
    [Google Scholar]
  121. 121. 
    Piálek L, Burress E, Dragová K, Almirón A, Casciotta J, Říčan O 2019. Phylogenomics of pike cichlids (Cichlidae: Crenicichla) of the C. mandelburgeri species complex: rapid ecological speciation in the Iguazú River and high endemism in the Middle Paraná basin. Hydrobiologia 832:355–75
    [Google Scholar]
  122. 122. 
    Richards EJ, Poelstra JW, Martin CH 2018. Don't throw out the sympatric speciation with the crater lake water: fine‐scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation. Evol. Lett. 2:5524–40
    [Google Scholar]
  123. 123. 
    Poelstra JW, Richards EJ, Martin CH 2018. Speciation in sympatry with ongoing secondary gene flow and a potential olfactory trigger in a radiation of Cameroon cichlids. Mol. Ecol. 27:214270–88
    [Google Scholar]
  124. 124. 
    Ballard JWO, Whitlock MC. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13:4729–44
    [Google Scholar]
  125. 125. 
    Joyce DA, Lunt DH, Genner MJ, Turner GF, Bills R, Seehausen O 2011. Repeated colonization and hybridization in Lake Malawi cichlids. Curr. Biol. 21:3R108–9
    [Google Scholar]
  126. 126. 
    Genner MJ, Turner GF. 2012. Ancient hybridization and phenotypic novelty within Lake Malawi's cichlid fish radiation. Mol. Biol. Evol. 29:1195–206
    [Google Scholar]
  127. 127. 
    Salzburger W, Baric S, Sturmbauer C 2002. Speciation via introgressive hybridization in East African cichlids. Mol. Ecol. 11:3619–25
    [Google Scholar]
  128. 128. 
    Stelkens RB, Schmid C, Selz O, Seehausen O 2009. Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish. BMC Evol. Biol. 9:283
    [Google Scholar]
  129. 129. 
    Nichols P, Genner MJ, van Oosterhout C, Smith A, Parsons P et al. 2015. Secondary contact seeds phenotypic novelty in cichlid fishes. Proc. R. Soc. B Biol. Sci. 282:179820142272
    [Google Scholar]
  130. 130. 
    Selz OM, Seehausen O. 2019. Interspecific hybridization can generate functional novelty in cichlid fish. Proc. R. Soc. B Biol. Sci. 286:20191621
    [Google Scholar]
  131. 131. 
    Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ et al. 2008. Speciation through sensory drive in cichlid fish. Nature 455:7213620–26
    [Google Scholar]
  132. 132. 
    Suarez-Gonzalez A, Lexer C, Cronk QCB 2018. Adaptive introgression: a plant perspective. Biol. Lett. 14:320170688
    [Google Scholar]
  133. 133. 
    Arnold ML, Kunte K. 2017. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32:8601–11
    [Google Scholar]
  134. 134. 
    Heliconius Genome Consort. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487:740594–98
    [Google Scholar]
  135. 135. 
    Huerta-Sánchez E, Jin X, Asan, Bianba Z, Peter BM et al. 2014. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512:7513194–97
    [Google Scholar]
  136. 136. 
    Meyer BS, Indermaur A, Ehrensperger X, Egger B, Banyankimbona G et al. 2015. Back to Tanganyika: a case of recent trans-species-flock dispersal in East African haplochromine cichlid fishes. R. Soc. Open Sci. 2:3140498
    [Google Scholar]
  137. 137. 
    1000 Genomes Proj. Consort Auton A, Brooks LD, Durbin RM, Garrison EP et al. 2015. A global reference for human genetic variation. Nature 526:757168–74
    [Google Scholar]
  138. 138. 
    Bergström A, McCarthy SA, Hui R, Almarri MA, Ayub Q et al. 2020. Insights into human genetic variation and population history from 929 diverse genomes. Science 367:6484eaay5012
    [Google Scholar]
  139. 139. 
    Ellegren H, Sheldon BC. 2008. Genetic basis of fitness differences in natural populations. Nature 452:7184169–75
    [Google Scholar]
  140. 140. 
    Dion-Côté A-M, Renaut S, Normandeau E, Bernatchez L 2014. RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. Mol. Biol. Evol. 31:51188–99
    [Google Scholar]
  141. 141. 
    Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N et al. 2012. Ancient admixture in human history. Genetics 192:31065–93
    [Google Scholar]
  142. 142. 
    Zheng Y, Janke A. 2018. Gene flow analysis method, the D-statistic, is robust in a wide parameter space. BMC Bioinform 19:10
    [Google Scholar]
  143. 143. 
    Eriksson A, Manica A. 2012. Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. PNAS 109:3513956–60
    [Google Scholar]
  144. 144. 
    Pease JB, Hahn MW. 2015. Detection and polarization of introgression in a five-taxon phylogeny. Syst. Biol. 64:4651–62
    [Google Scholar]
  145. 145. 
    Malinsky M, Matschiner M, Svardal H 2020. Dsuite - fast D-statistics and related admixture evidence from VCF files. Mol. Ecol. Res. https://doi.org/10.1111/1755-0998.13265
    [Crossref] [Google Scholar]
  146. 146. 
    Lawson DJ, Hellenthal G, Myers S, Falush D 2012. Inference of population structure using dense haplotype data. PLOS Genet 8:1e1002453
    [Google Scholar]
  147. 147. 
    Malinsky M, Trucchi E, Lawson DJ, Falush D 2018. RADpainter and fineRADstructure: population inference from RADseq data. Mol. Biol. Evol. 35:51284–90
    [Google Scholar]
  148. 148. 
    Kautt A, Kratochwil C, Nater A, Machado-Schiaffino G, Olave Met al 2020. Contrasting signatures of genomic divergence during sympatric speciation. Nature 588:106–11
    [Google Scholar]
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