1932

Abstract

The repeated adaptation of oceanic threespine sticklebacks to fresh water has made it a premier organism to study parallel evolution. These small fish have multiple distinct ecotypes that display a wide range of diverse phenotypic traits. Ecotypes are easily crossed in the laboratory, and families are large and develop quickly enough for quantitative trait locus analyses, positioning the threespine stickleback as a versatile model organism to address a wide range of biological questions. Extensive genomic resources, including linkage maps, a high-quality reference genome, and developmental genetics tools have led to insights into the genomic basis of adaptation and the identification of genomic changes controlling traits in vertebrates. Recently, threespine sticklebacks have been used as a model system to identify the genomic basis of highly complex traits, such as behavior and host–microbiome and host–parasite interactions. We review the latest findings and new avenues of research that have led the threespine stickleback to be considered a supermodel of evolutionary genomics.

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2021-08-31
2024-04-24
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Literature Cited

  1. 1. 
    Aguirre WE, Bell MA. 2012. Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment. Biol. J. Linn. Soc. Lond. 105:817–31
    [Google Scholar]
  2. 2. 
    Albert AYK, Sawaya S, Vines TH, Knecht AK, Miller CT et al. 2008. The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62:76–85
    [Google Scholar]
  3. 3. 
    Althani AA, Marei HE, Hamdi WS, Nasrallah GK, El Zowalaty ME et al. 2016. Human microbiome and its association with health and diseases. J. Cell. Physiol. 231:1688–94
    [Google Scholar]
  4. 4. 
    Archambeault SL, Bärtschi LR, Merminod AD, Peichel CL. 2020. Adaptation via pleiotropy and linkage: association mapping reveals a complex genetic architecture within the stickleback Eda locus. Evol. Lett. 4:282–301
    [Google Scholar]
  5. 5. 
    Artemov AV, Mugue NS, Rastorguev SM, Zhenilo S, Mazur AM et al. 2017. Genome-wide DNA methylation profiling reveals epigenetic adaptation of stickleback to marine and freshwater conditions. Mol. Biol. Evol. 34:2203–13
    [Google Scholar]
  6. 6. 
    Barber I. 2013. Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends Parasitol 29:556–66
    [Google Scholar]
  7. 7. 
    Barber I, Scharsack JP. 2010. The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137:411–24
    [Google Scholar]
  8. 8. 
    Barghi N, Hermisson J, Schlötterer C. 2020. Polygenic adaptation: a unifying framework to understand positive selection. Nat. Rev. Genet. 21:769–81
    [Google Scholar]
  9. 9. 
    Barghi N, Tobler R, Nolte V, Jakšić AM, Mallard F et al. 2019. Genetic redundancy fuels polygenic adaptation in Drosophila. PLOS Biol. 17:e3000128
    [Google Scholar]
  10. 10. 
    Barrett RDH, Schluter D. 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:38–44
    [Google Scholar]
  11. 11. 
    Bassham S, Catchen J, Lescak E, von Hippel FA, Cresko WA. 2018. Repeated selection of alternatively adapted haplotypes creates sweeping genomic remodeling in stickleback. Genetics 209:921–39
    [Google Scholar]
  12. 12. 
    Beck EA, Currey MC, Small CM, Cresko WA 2020. QTL mapping of intestinal neutrophil variation in threespine stickleback reveals possible gene targets connecting intestinal inflammation and systemic health. G3 10:613–22
    [Google Scholar]
  13. 13. 
    Bell AM, Bukhari SA, Sanogo YO. 2016. Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks. Behaviour 153:1723–43
    [Google Scholar]
  14. 14. 
    Bell AM, Trapp R, Keagy J. 2018. Parenting behaviour is highly heritable in male stickleback. R. Soc. Open Sci. 5:171029
    [Google Scholar]
  15. 15. 
    Bell MA. 1976. Evolution of phenotypic diversity in Gasterosteus aculeatus superspecies on the Pacific coast of North America. Syst. Zool. 25:211–27
    [Google Scholar]
  16. 16. 
    Bell MA 1984. Evolutionary phenetics and genetics. Evolutionary Genetics of Fishes BJ Turner 431–528 New York: Plenum
    [Google Scholar]
  17. 17. 
    Bell MA. 1995. Sticklebacks: a model for behavior evolution. Trends Ecol. Evol. 10:101–3
    [Google Scholar]
  18. 18. 
    Bell MA. 2009. Implications of a fossil stickleback assemblage for Darwinian gradualism. J. Fish Biol. 75:1977–99
    [Google Scholar]
  19. 19. 
    Bell MA. 2010. Miocene and Late Pleistocene stickleback spines from the Mojave Desert, California. Overboard in the Mojave: 20 Million Years of Lakes and Wetlands RE Reynolds, DM Miller 162–68 Yucca Valley, CA: Desert Symp.
    [Google Scholar]
  20. 20. 
    Bell MA, Aguirre WE. 2013. Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback. Evol. Ecol. Res. 15:377–411
    [Google Scholar]
  21. 21. 
    Bell MA, Foster SA 1994. Introduction to the evolutionary biology of the threespine stickleback. The Evolutionary Biology of the Threespine Stickleback MA Bell, SA Foster 1–27 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  22. 22. 
    Bell MA, Stewart JD, Park PJ. 2009. The world's oldest fossil threespine stickleback fish. Copeia 2009:256–65
    [Google Scholar]
  23. 23. 
    Bengston SE, Dahan RA, Donaldson Z, Phelps SM, van Oers K et al. 2018. Genomic tools for behavioural ecologists to understand repeatable individual differences in behaviour. Nat. Ecol. Evol. 2:944–55
    [Google Scholar]
  24. 24. 
    Blount ZD, Lenski RE, Losos JB. 2018. Contingency and determinism in evolution: replaying life's tape. Science 362:eaam5979
    [Google Scholar]
  25. 25. 
    Bolnick DI, Snowberg LK, Caporaso JG, Lauber C, Knight R, Stutz WE. 2014. Major Histocompatibility Complex class IIb polymorphism influences gut microbiota composition and diversity. Mol. Ecol. 23:4831–45
    [Google Scholar]
  26. 26. 
    Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R et al. 2014. Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol. Lett. 17:979–87
    [Google Scholar]
  27. 27. 
    Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E et al. 2014. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat. Commun. 5:4500
    [Google Scholar]
  28. 28. 
    Bubac CM, Miller JM, Coltman DW. 2020. The genetic basis of animal behavioural diversity in natural populations. Mol. Ecol. 29:1957–71
    [Google Scholar]
  29. 29. 
    Bukhari SA, Saul MC, James N, Bensky MK, Stein LR et al. 2019. Neurogenomic insights into paternal care and its relation to territorial aggression. Nat. Commun. 10:4437
    [Google Scholar]
  30. 30. 
    Bukhari SA, Saul MC, Seward CH, Zhang H, Bensky M et al. 2017. Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks. PLOS Genet 13:e1006840
    [Google Scholar]
  31. 31. 
    Chain FJJ, Feulner PGD, Panchal M, Eizaguirre C, Samonte IE et al. 2014. Extensive copy-number variation of young genes across stickleback populations. PLOS Genet 10:e1004830
    [Google Scholar]
  32. 32. 
    Chan YF, Marks ME, Jones FC, Villarreal G Jr., Shapiro MD et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–5
    [Google Scholar]
  33. 33. 
    Cleves PA, Ellis NA, Jimenez MT, Nunez SM, Schluter D et al. 2014. Evolved tooth gain in sticklebacks is associated with a cis-regulatory allele of Bmp6. PNAS 111:13912–17
    [Google Scholar]
  34. 34. 
    Cleves PA, Hart JC, Agoglia RM, Jimenez MT, Erickson PA et al. 2018. An intronic enhancer of Bmp6 underlies evolved tooth gain in sticklebacks. PLOS Genet 14:e1007449
    [Google Scholar]
  35. 35. 
    Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr., Dickson M et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307:1928–33
    [Google Scholar]
  36. 36. 
    Colosimo PF, Peichel CL, Nereng K, Blackman BK, Shapiro MD et al. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLOS Biol 2:e109
    [Google Scholar]
  37. 37. 
    Conte GL, Arnegard ME, Best J, Chan YF, Jones FC et al. 2015. Extent of QTL reuse during repeated phenotypic divergence of sympatric threespine stickleback. Genetics 201:1189–200
    [Google Scholar]
  38. 38. 
    Cresko WA, Amores A, Wilson C, Murphy J, Currey M et al. 2004. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. PNAS 101:6050–55
    [Google Scholar]
  39. 39. 
    Cresko WA, McGuigan KL, Phillips PC, Postlethwait JH. 2007. Studies of threespine stickleback developmental evolution: progress and promise. Genetica 129:105–26
    [Google Scholar]
  40. 40. 
    Deagle BE, Jones FC, Chan YF, Absher DM, Kingsley DM, Reimchen TE. 2012. Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions. Proc. R. Soc. B 279:1277–86
    [Google Scholar]
  41. 41. 
    Dittmar EL, Oakley CG, Conner JK, Gould BA, Schemske DW. 2016. Factors influencing the effect size distribution of adaptive substitutions. Proc. R. Soc. B 283:20153065
    [Google Scholar]
  42. 42. 
    Douglas AE. 2019. Simple animal models for microbiome research. Nat. Rev. Microbiol. 17:764–75
    [Google Scholar]
  43. 43. 
    Eizaguirre C, Lenz TL, Kalbe M, Milinski M. 2012. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat. Commun. 3:621
    [Google Scholar]
  44. 44. 
    Erickson PA, Baek J, Hart JC, Cleves PA, Miller CT. 2018. Genetic dissection of a supergene implicates Tfap2a in craniofacial evolution of threespine sticklebacks. Genetics 209:591–605
    [Google Scholar]
  45. 45. 
    Erickson PA, Glazer AM, Killingbeck EE, Agoglia RM, Baek J et al. 2016. Partially repeatable genetic basis of benthic adaptation in threespine sticklebacks. Evolution 70:887–902
    [Google Scholar]
  46. 46. 
    Fang B, Kemppainen P, Momigliano P, Feng X, Merilä J. 2020. On the causes of geographically heterogeneous parallel evolution in sticklebacks. Nat. Ecol. Evol. 4:1105–15
    [Google Scholar]
  47. 47. 
    Fang B, Kemppainen P, Momigliano P, Merilä J. 2021. Population structure limits parallel evolution. bioRxiv 2021.01.26.428263. https://doi.org/10.1101/2021.01.26.428263
    [Crossref] [Google Scholar]
  48. 48. 
    Fang B, Merilä J, Matschiner M, Momigliano P. 2020. Estimating uncertainty in divergence times among three-spined stickleback clades using the multispecies coalescent. Mol. Phylogenet. Evol. 142:106646
    [Google Scholar]
  49. 49. 
    Feulner PGD, Chain FJJ, Panchal M, Huang Y, Eizaguirre C et al. 2015. Genomics of divergence along a continuum of parapatric population differentiation. PLOS Genet 11:e1004966
    [Google Scholar]
  50. 50. 
    Fisher RA. 2009 (1930). The Genetical Theory of Natural Selection: A Complete Variorum Edition Oxford, UK: Oxford Univ. Press
  51. 51. 
    Friberg IM, Taylor JD, Jackson JA. 2019. Diet in the driving seat: natural diet-immunity-microbiome interactions in wild fish. Front. Immunol. 10:243
    [Google Scholar]
  52. 52. 
    Fuess L, den Haan S, Ling F, Weber JN, Steinel NC, Bolnick DI. 2020. Immune gene expression covaries with gut microbiome composition in stickleback. bioRxiv 2020.08.04.236786. https://doi.org/10.1101/2020.08.04.236786
    [Crossref] [Google Scholar]
  53. 53. 
    Galloway J, Cresko WA, Ralph P. 2020. A few stickleback suffice for the transport of alleles to new lakes. G3 10:505–14
    [Google Scholar]
  54. 54. 
    Gambling SJ, Reimchen TE. 2012. Prolonged life span among endemic Gasterosteus populations. Can. J. Zool. 90:284–90
    [Google Scholar]
  55. 55. 
    Glazer AM, Cleves PA, Erickson PA, Lam AY, Miller CT. 2014. Parallel developmental genetic features underlie stickleback gill raker evolution. EvoDevo 5:19
    [Google Scholar]
  56. 56. 
    Glazer AM, Killingbeck EE, Mitros T, Rokhsar DS, Miller CT. 2015. Genome assembly improvement and mapping convergently evolved skeletal traits in sticklebacks with genotyping-by-sequencing. G3 5:1463–72
    [Google Scholar]
  57. 57. 
    Gow JL, Peichel CL, Taylor EB. 2007. Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. J. Evol. Biol. 20:2173–80
    [Google Scholar]
  58. 58. 
    Greenwood AK, Mills MG, Wark AR, Archambeault SL, Peichel CL. 2016. Evolution of schooling behavior in threespine sticklebacks is shaped by the Eda gene. Genetics 203:677–81
    [Google Scholar]
  59. 59. 
    Greenwood AK, Peichel CL. 2015. Social regulation of gene expression in threespine sticklebacks. PLOS ONE 10:e0137726
    [Google Scholar]
  60. 60. 
    Greenwood AK, Wark AR, Yoshida K, Peichel CL. 2013. Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks. Curr. Biol. 23:1884–88
    [Google Scholar]
  61. 61. 
    Guo B, DeFaveri J, Sotelo G, Nair A, Merilä J. 2015. Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks. BMC Biol. 13:19
    [Google Scholar]
  62. 62. 
    Hagen DW. 1967. Isolating mechanisms in threespine sticklebacks (Gasterosteus). J. Fish. Res. Board Can. 24:1637–92
    [Google Scholar]
  63. 63. 
    Hagen DW, Gilbertson LG. 1973. Selective predation and the intensity of selection acting upon the lateral plates of threespine sticklebacks. Heredity 30:273–87
    [Google Scholar]
  64. 64. 
    Hahn MA, Rosario K, Lucas P, Dheilly NM. 2020. Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host. ISME J 14:1755–67
    [Google Scholar]
  65. 65. 
    Harris RM, Hofmann HA. 2014. Neurogenomics of behavioral plasticity. Adv. Exp. Med. Biol. 781:149–68
    [Google Scholar]
  66. 66. 
    Hart JC, Miller CT. 2017. Sequence-based mapping and genome editing reveal mutations in stickleback Hps5 cause oculocutaneous albinism and the casper phenotype. G3 7:3123–31
    [Google Scholar]
  67. 67. 
    Heckwolf MJ, Meyer BS, Häsler R, Höppner MP, Eizaguirre C, Reusch TBH. 2020. Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation. Sci. Adv 6:eaaz1138
    [Google Scholar]
  68. 68. 
    Heins D, Baker J. 2008. The stickleback–Schistocephalus host–parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145:625–45
    [Google Scholar]
  69. 69. 
    Hendry AP, Bolnick DI, Berner D, Peichel CL. 2009. Along the speciation continuum in sticklebacks. J. Fish Biol. 75:2000–36
    [Google Scholar]
  70. 70. 
    Hendry AP, Peichel CL, Matthews B, Boughman JW, Nosil P. 2013. Stickleback research: the now and the next. Evol. Ecol. Res. 15:111–41
    [Google Scholar]
  71. 71. 
    Hermisson J, Pennings PS. 2005. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169:2335–52
    [Google Scholar]
  72. 72. 
    Hernandez RD, Kelley JL, Elyashiv E, Melton SC, Auton A et al. 2011. Classic selective sweeps were rare in recent human evolution. Science 331:920–24
    [Google Scholar]
  73. 73. 
    Hoekstra HE, Coyne JA. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61:995–1016
    [Google Scholar]
  74. 74. 
    Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLOS Genet 6:e1000862
    [Google Scholar]
  75. 75. 
    Hohenlohe PA, Magalhaes IS 2020. The population genomics of parallel adaptation: lessons from threespine stickleback. Population Genomics: Marine Organisms MF Oleksiak, OP Rajora 249–76 Cham, Switz: Springer
    [Google Scholar]
  76. 76. 
    Howes TR, Summers BR, Kingsley DM. 2017. Dorsal spine evolution in threespine sticklebacks via a splicing change in MSX2A. BMC Biol 15:115
    [Google Scholar]
  77. 77. 
    Huntingford FA, Ruiz-Gomez ML. 2009. Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology. J. Fish Biol. 75:1943–76
    [Google Scholar]
  78. 78. 
    Indjeian VB, Kingman GA, Jones FC, Guenther CA, Grimwood J et al. 2016. Evolving new skeletal traits by cis-regulatory changes in bone morphogenetic proteins. Cell 164:45–56
    [Google Scholar]
  79. 79. 
    Jain K, Stephan W 2017. Modes of rapid polygenic adaptation. Mol. Biol. Evol. 34:3169–75
    [Google Scholar]
  80. 80. 
    James N, Bell A. 2020. Minimally invasive brain injections for viral-mediated transgenesis: new tools for behavioral genetics in sticklebacks. bioRxiv 2020.03.02.973594. https://doi.org/10.1101/2020.03.02.973594
    [Crossref]
  81. 81. 
    Jamieson IG, Blouw DM, Colgan PW. 1992. Parental care as a constraint on male mating success in fishes: a comparative study of threespine and white sticklebacks. Can. J. Zool. 70:956–62
    [Google Scholar]
  82. 82. 
    Jolles JW, Mazué GPF, Davidson J, Behrmann-Godel J, Couzin ID. 2020. Schistocephalus parasite infection alters sticklebacks’ movement ability and thereby shapes social interactions. Sci. Rep. 10:12282
    [Google Scholar]
  83. 83. 
    Jones FC, Chan YF, Schmutz J, Grimwood J, Brady SD et al. 2012. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr. Biol. 22:83–90
    [Google Scholar]
  84. 84. 
    Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61
    [Google Scholar]
  85. 85. 
    Kawahara R, Miya M, Mabuchi K, Near TJ, Nishida M. 2009. Stickleback phylogenies resolved: evidence from mitochondrial genomes and 11 nuclear genes. Mol. Phylogenet. Evol. 50:401–4
    [Google Scholar]
  86. 86. 
    Kingsley DM. 2003. Sequencing the genome of threespine sticklebacks (Gasterosteus aculeatus) White Pap., Natl. Hum. Genome Res. Inst. Bethesda, MD:
    [Google Scholar]
  87. 87. 
    Kingsley DM, Zhu B, Osoegawa K, De Jong PJ, Schein J et al. 2004. New genomic tools for molecular studies of evolutionary change in threespine sticklebacks. Behaviour 141:1331–44
    [Google Scholar]
  88. 88. 
    Klepaker T. 1993. Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can. J. Zool. 71:1251–58
    [Google Scholar]
  89. 89. 
    Laurentino TG, Moser D, Roesti M, Ammann M, Frey A et al. 2020. Genomic release-recapture experiment in the wild reveals within-generation polygenic selection in stickleback fish. Nat. Commun. 11:1928
    [Google Scholar]
  90. 90. 
    Lescak EA, Bassham SL, Catchen J, Gelmond O, Sherbick ML et al. 2015. Evolution of stickleback in 50 years on earthquake-uplifted islands. PNAS 112:E7204–12
    [Google Scholar]
  91. 91. 
    Lescak EA, Milligan-Myhre KC. 2017. Teleosts as model organisms to understand host-microbe interactions. J. Bacteriol. 199:e00868–16
    [Google Scholar]
  92. 92. 
    Ling F, Steinel N, Weber J, Ma L, Smith C et al. 2020. The gut microbiota response to helminth infection depends on host sex and genotype. ISME J 14:1141–53
    [Google Scholar]
  93. 93. 
    Lohman BK, Steinel NC, Weber JN, Bolnick DI. 2017. Gene expression contributes to the recent evolution of host resistance in a model host parasite system. Front. Immunol. 8:1071
    [Google Scholar]
  94. 94. 
    Lowe CB, Sanchez-Luege N, Howes TR, Brady SD, Daugherty RR et al. 2018. Detecting differential copy number variation between groups of samples. Genome Res 28:256–65
    [Google Scholar]
  95. 95. 
    MacColl ADC. 2009. Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32:153–60
    [Google Scholar]
  96. 96. 
    Marques DA, Jones FC, Di Palma F, Kingsley DM, Reimchen TE. 2018. Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation. Nat. Ecol. Evol. 2:1128–38
    [Google Scholar]
  97. 97. 
    Marques DA, Lucek K, Meier JI, Mwaiko S, Wagner CE et al. 2016. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLOS Genet 12:e1005887
    [Google Scholar]
  98. 98. 
    Marques DA, Taylor JS, Jones FC, Di Palma F, Kingsley DM, Reimchen TE. 2017. Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments. PLOS Biol. 15:e2001627
    [Google Scholar]
  99. 99. 
    Matuszewski S, Hermisson J, Kopp M. 2015. Catch me if you can: adaptation from standing genetic variation to a moving phenotypic optimum. Genetics 200:1255–74
    [Google Scholar]
  100. 100. 
    McGee MD, Borstein SR, Meier JI, Marques DA, Mwaiko S et al. 2020. The ecological and genomic basis of explosive adaptive radiation. Nature 586:75–79
    [Google Scholar]
  101. 101. 
    McGhee KE, Bell AM. 2014. Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety. Proc. R. Soc. B 281:20141146
    [Google Scholar]
  102. 102. 
    McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG et al. 2007. Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448:587–90
    [Google Scholar]
  103. 103. 
    McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM et al. 2004. Evidence for ecology's role in speciation. Nature 429:294–98
    [Google Scholar]
  104. 104. 
    McKinnon JS, Rundle HD. 2002. Speciation in nature: the threespine stickleback model systems. Trends Ecol. Evol. 17:480–88
    [Google Scholar]
  105. 105. 
    McPhail JD. 1969. Predation and the evolution of a stickleback (Gasterosteus). J. Fish. Res. Board Can. 26:3183–208
    [Google Scholar]
  106. 106. 
    McPhail JD. 1993. Ecology and evolution of sympatric sticklebacks (Gasterosteus): origin of the species pairs. Can. J. Zool. 71:515–23
    [Google Scholar]
  107. 107. 
    Milinski M, Bakker TCM. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–33
    [Google Scholar]
  108. 108. 
    Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA et al. 2007. cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131:1179–89
    [Google Scholar]
  109. 109. 
    Miller CT, Glazer AM, Summers BR, Blackman BK, Norman AR et al. 2014. Modular skeletal evolution in sticklebacks is controlled by additive and clustered quantitative trait loci. Genetics 197:405–20
    [Google Scholar]
  110. 110. 
    Milligan-Myhre K, Small CM, Mittge EK, Agarwal M, Currey M et al. 2016. Innate immune responses to gut microbiota differ between oceanic and freshwater threespine stickleback populations. Dis. Model. Mech. 9:187–98
    [Google Scholar]
  111. 111. 
    Mills MG, Greenwood AK, Peichel CL. 2014. Pleiotropic effects of a single gene on skeletal development and sensory system patterning in sticklebacks. EvoDevo 5:5
    [Google Scholar]
  112. 112. 
    Nath S, Shaw DE, White MA. 2021. Improved contiguity of the threespine stickleback genome using long-read sequencing. G3 11:jkab007
    [Google Scholar]
  113. 113. 
    Nazarkin MV, Yabumoto Y, Urabe A. 2013. A new Miocene three-spined stickleback (Pisces: Gasterosteidae) from central Japan. Paleontol. Res. 16:318–28
    [Google Scholar]
  114. 114. 
    Nelson TC, Crandall JG, Ituarte CM, Catchen JM, Cresko WA. 2019. Selection, linkage, and population structure interact to shape genetic variation among threespine stickleback genomes. Genetics 212:1367–82
    [Google Scholar]
  115. 115. 
    Nelson TC, Cresko WA. 2018. Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations. Evol. Lett. 2:9–21
    [Google Scholar]
  116. 116. 
    Niepoth N, Bendesky A. 2020. How natural genetic variation shapes behavior. Annu. Rev. Genom. Hum. Genet. 21:437–63
    [Google Scholar]
  117. 117. 
    O'Brown NM, Summers BR, Jones FC, Brady SD, Kingsley DM. 2015. A recurrent regulatory change underlying altered expression and Wnt response of the stickleback armor plates gene EDA. eLife 4:e05290
    [Google Scholar]
  118. 118. 
    Oke KB, Bukhari M, Kaeuffer R, Rolshausen G, Räsänen K et al. 2016. Does plasticity enhance or dampen phenotypic parallelism? A test with three lake–stream stickleback pairs. J. Evol. Biol. 29:126–43
    [Google Scholar]
  119. 119. 
    Orr HA. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52:935–49
    [Google Scholar]
  120. 120. 
    Orr HA. 2005. Theories of adaptation: what they do and don't say. Genetica 123:3–13
    [Google Scholar]
  121. 121. 
    Ostrander EA, Wayne RK. 2005. The canine genome. Genome Res 15:1706–16
    [Google Scholar]
  122. 122. 
    Pearse DE, Barson NJ, Nome T, Gao G, Campbell MA et al. 2019. Sex-dependent dominance maintains migration supergene in rainbow trout. Nat. Ecol. Evol. 3:1731–42
    [Google Scholar]
  123. 123. 
    Peichel CL, Marques DA. 2017. The genetic and molecular architecture of phenotypic diversity in sticklebacks. Philos. Trans. R. Soc. Lond. B 372:20150486
    [Google Scholar]
  124. 124. 
    Peichel CL, McCann SR, Ross JA, Naftaly AFS, Urton JR et al. 2020. Assembly of the threespine stickleback Y chromosome reveals convergent signatures of sex chromosome evolution. Genome Biol 21:177
    [Google Scholar]
  125. 125. 
    Peichel CL, Nereng KS, Ohgi KA, Cole BL, Colosimo PF et al. 2001. The genetic architecture of divergence between threespine stickleback species. Nature 414:901–5
    [Google Scholar]
  126. 126. 
    Peichel CL, Sullivan ST, Liachko I, White MA. 2017. Improvement of the threespine stickleback genome using a Hi-C-based proximity-guided assembly. J. Hered. 108:693–700
    [Google Scholar]
  127. 127. 
    Pritchard JK, Pickrell JK, Coop G. 2010. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 20:R208–15
    [Google Scholar]
  128. 128. 
    Pritchard VL, Viitaniemi HM, McCairns RJS, Merilä J, Nikinmaa M et al. 2017. Regulatory architecture of gene expression variation in the threespine stickleback Gasterosteus aculeatus. G3 7:165–78
    [Google Scholar]
  129. 129. 
    Przeworski M, Coop G, Wall JD. 2005. The signature of positive selection on standing genetic variation. Evolution 59:2312–23
    [Google Scholar]
  130. 130. 
    Rennison DJ, Rudman SM, Schluter D. 2019. Parallel changes in gut microbiome composition and function during colonization, local adaptation and ecological speciation. Proc. R. Soc. B 286:20191911
    [Google Scholar]
  131. 131. 
    Rittschof CC, Bukhari SA, Sloofman LG, Troy JM, Caetano-Anollés D et al. 2014. Neuromolecular responses to social challenge: common mechanisms across mouse, stickleback fish, and honey bee. PNAS 111:17929–34
    [Google Scholar]
  132. 132. 
    Roberts Kingman GA, Vyas DN, Jones FC, Brady SD, Chen HIet al 2021. Predicting future from past: the genomic basis of recurrent and rapid stickleback evolution. Sci. Adv 7:eabg5285
    [Google Scholar]
  133. 133. 
    Robertson RC, Manges AR, Finlay BB, Prendergast AJ. 2019. The human microbiome and child growth—first 1000 days and beyond. Trends Microbiol 27:131–47
    [Google Scholar]
  134. 134. 
    Roesti M, Kueng B, Moser D, Berner D. 2015. The genomics of ecological vicariance in threespine stickleback fish. Nat. Commun. 6:8767
    [Google Scholar]
  135. 135. 
    Roesti M, Moser D, Berner D. 2013. Recombination in the threespine stickleback genome—patterns and consequences. Mol. Ecol. 22:3014–27
    [Google Scholar]
  136. 136. 
    Rundle HD, Nagel L, Boughman JW, Schluter D. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306–8
    [Google Scholar]
  137. 137. 
    Sagonas K, Meyer BS, Kaufmann J, Lenz TL, Häsler R, Eizaguirre C. 2020. Experimental parasite infection causes genome-wide changes in DNA methylation. Mol. Biol. Evol. 37:2287–99
    [Google Scholar]
  138. 138. 
    Sanogo YO, Band M, Blatti C, Sinha S, Bell AM. 2012. Transcriptional regulation of brain gene expression in response to a territorial intrusion. Proc. R. Soc. B 279:4929–38
    [Google Scholar]
  139. 139. 
    Sanogo YO, Bell AM. 2016. Molecular mechanisms and the conflict between courtship and aggression in three-spined sticklebacks. Mol. Ecol. 25:4368–76
    [Google Scholar]
  140. 140. 
    Sanogo YO, Hankison S, Band M, Obregon A, Bell AM. 2011. Brain transcriptomic response of threespine sticklebacks to cues of a predator. Brain Behav. Evol. 77:270–85
    [Google Scholar]
  141. 141. 
    Saul MC, Blatti C, Yang W, Bukhari SA, Shpigler HY et al. 2019. Cross-species systems analysis of evolutionary toolkits of neurogenomic response to social challenge. Genes Brain Behav 18:e12502
    [Google Scholar]
  142. 142. 
    Schluter D, Conte GL. 2009. Genetics and ecological speciation. PNAS 106:Suppl. 19955–62
    [Google Scholar]
  143. 143. 
    Schluter D, Marchinko KB, Arnegard ME, Zhang H, Brady SD et al. 2021. Fitness maps to a large-effect locus in introduced stickleback populations. PNAS 118:e1914889118
    [Google Scholar]
  144. 144. 
    Schwander T, Libbrecht R, Keller L. 2014. Supergenes and complex phenotypes. Curr. Biol. 24:R288–94
    [Google Scholar]
  145. 145. 
    Sella G, Barton NH. 2019. Thinking about the evolution of complex traits in the era of genome-wide association studies. Annu. Rev. Genom. Hum. Genet. 20:461–93
    [Google Scholar]
  146. 146. 
    Shanfelter AF, Archambeault SL, White MA. 2019. Divergent fine-scale recombination landscapes between a freshwater and marine population of threespine stickleback fish. Genome Biol. Evol. 11:1522–27
    [Google Scholar]
  147. 147. 
    Shapiro MD, Bell MA, Kingsley DM. 2006. Parallel genetic origins of pelvic reduction in vertebrates. PNAS 103:13753–58
    [Google Scholar]
  148. 148. 
    Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS et al. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–23
    [Google Scholar]
  149. 149. 
    Small CM, Milligan-Myhre K, Bassham S, Guillemin K, Cresko WA. 2017. Host genotype and microbiota contribute asymmetrically to transcriptional variation in the threespine stickleback gut. Genome Biol. Evol. 9:504–20
    [Google Scholar]
  150. 150. 
    Smith CCR, Snowberg LK, Gregory Caporaso J, Knight R, Bolnick DI 2015. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J 9:2515–26
    [Google Scholar]
  151. 151. 
    Stein LR, Bell AM. 2012. Consistent individual differences in fathering in threespined stickleback Gasterosteus aculeatus. Curr. Zool. 58:45–52
    [Google Scholar]
  152. 152. 
    Stein LR, Bell AM. 2015. Consistent individual differences in paternal behavior: a field study of three-spined stickleback. Behav. Ecol. Sociobiol. 69:227–36
    [Google Scholar]
  153. 153. 
    Steury RA, Currey MC, Cresko WA, Bohannan BJM. 2019. Population genetic divergence and environment influence the gut microbiome in Oregon threespine stickleback. Genes 10:484
    [Google Scholar]
  154. 154. 
    Stewart A, Jackson J, Barber I, Eizaguirre C, Paterson R et al. 2017. Hook, line and infection: a guide to culturing parasites, establishing infections and assessing immune responses in the three-spined stickleback. Adv. Parasitol. 98:39–109
    [Google Scholar]
  155. 155. 
    Stuart YE, Travis MP, Bell MA. 2020. Inferred genetic architecture underlying evolution in a fossil stickleback lineage. Nat. Ecol. Evol. 4:1549–57
    [Google Scholar]
  156. 156. 
    Stuart YE, Veen T, Weber JN, Hanson D, Ravinet M et al. 2017. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat. Ecol. Evol. 1:158
    [Google Scholar]
  157. 157. 
    Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL. 2006. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol. Ecol. 15:343–55
    [Google Scholar]
  158. 158. 
    Terekhanova NV, Logacheva MD, Penin AA, Neretina TV, Barmintseva AE et al. 2014. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLOS Genet 10:e1004696
    [Google Scholar]
  159. 159. 
    Thompson AC, Capellini TD, Guenther CA, Chan YF, Infante CR et al. 2018. A novel enhancer near the Pitx1 gene influences development and evolution of pelvic appendages in vertebrates. eLife 7:e38555
    [Google Scholar]
  160. 160. 
    Thompson KA, Osmond MM, Schluter D. 2019. Parallel genetic evolution and speciation from standing variation. Evol. Lett. 3:129–41
    [Google Scholar]
  161. 161. 
    Tinbergen N. 1951. The Study of Instinct, Vol. 237 Oxford, UK: Clarendon
  162. 162. 
    Todesco M, Owens GL, Bercovich N, Légaré J-S, Soudi S et al. 2020. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature 584:602–7
    [Google Scholar]
  163. 163. 
    Verta J-P, Jones FC. 2019. Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks. eLife 8:e43785
    [Google Scholar]
  164. 164. 
    Wark AR, Greenwood AK, Taylor EM, Yoshida K, Peichel CL. 2011. Heritable differences in schooling behavior among threespine stickleback populations revealed by a novel assay. PLOS ONE 6:e18316
    [Google Scholar]
  165. 165. 
    Weber JN, Kalbe M, Shim KC, Erin NI, Steinel NC et al. 2017. Resist globally, infect locally: a transcontinental test of adaptation by stickleback and their tapeworm parasite. Am. Nat. 189:43–57
    [Google Scholar]
  166. 166. 
    Wellenreuther M, Bernatchez L. 2018. Eco-evolutionary genomics of chromosomal inversions. Trends Ecol. Evol. 33:427–40
    [Google Scholar]
  167. 167. 
    Wootton RJ. 1984. A Functional Biology of Sticklebacks Berkeley: Univ. Calif. Press
  168. 168. 
    Wucherpfennig JI, Miller CT, Kingsley DM. 2019. Efficient CRISPR-Cas9 editing of major evolutionary loci in sticklebacks. Evol. Ecol. Res. 20:107–32
    [Google Scholar]
  169. 169. 
    Xie KT, Wang G, Thompson AC, Wucherpfennig JI, Reimchen TE et al. 2019. DNA fragility in the parallel evolution of pelvic reduction in stickleback fish. Science 363:81–84
    [Google Scholar]
  170. 170. 
    Yoshida K, Makino T, Yamaguchi K, Shigenobu S, Hasebe M et al. 2014. Sex chromosome turnover contributes to genomic divergence between incipient stickleback species. PLOS Genet 10:e1004223
    [Google Scholar]
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