Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

The genomics of coloration provides insights into adaptive evolution

A Publisher Correction to this article was published on 18 May 2020

This article has been updated

Abstract

Coloration is an easily quantifiable visual trait that has proven to be a highly tractable system for genetic analysis and for studying adaptive evolution. The application of genomic approaches to evolutionary studies of coloration is providing new insight into the genetic architectures underlying colour traits, including the importance of large-effect mutations and supergenes, the role of development in shaping genetic variation and the origins of adaptive variation, which often involves adaptive introgression. Improved knowledge of the genetic basis of traits can facilitate field studies of natural selection and sexual selection, making it possible for strong selection and its influence on the genome to be demonstrated in wild populations.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Different ways of making colour.
Fig. 2: Signalling through colour.
Fig. 3: Genetic architecture of colour loci.
Fig. 4: Development can shape evolution.
Fig. 5: An introgressed allele is responsible for the loss of phenotypic plasticity in snowshoe hares.
Fig. 6: Estimating natural selection.

Similar content being viewed by others

Change history

References

  1. Cuthill, I. C. et al. The biology of color. Science 357, eaan0221 (2017).

    PubMed  Google Scholar 

  2. Protas, M. E. & Patel, N. H. Evolution of coloration patterns. Annu. Rev. Cell Dev. Biol. 24, 425–446 (2008).

    CAS  PubMed  Google Scholar 

  3. Quicke, D. L. J. Mimicry, Crypsis, Masquerade and Other Adaptive Resemblances (Wiley, 2017).

  4. Caro, T. & Allen, W. L. Interspecific visual signalling in animals and plants: a functional classification. Phil. Trans. R. Soc. B Biol. Sci. 372, 20160344 (2017).

    Google Scholar 

  5. Hill, G. E., Hill, G. E. & McGraw, K. J. Bird Coloration: Function and Evolution (Harvard Univ. Press, 2006).

  6. Andrade, P. et al. Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proc. Natl Acad. Sci. USA 116, 5633–5642 (2019). This study identifies two genes that underlie red, orange and yellow pigmentation in the wall lizard. The colour morphs also differ in their physiology and behaviour and the identified loci are candidates for involvement in those traits.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Shawkey, M. D. & Hill, G. E. Carotenoids need structural colours to shine. Biol. Lett. 1, 121–124 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Shawkey, M. D., Morehouse, N. I. & Vukusic, P. A protean palette: colour materials and mixing in birds and butterflies. J. R. Soc. Interface 6, S221–S231 (2009).

    PubMed  PubMed Central  Google Scholar 

  9. Cooke, T. F. et al. Genetic mapping and biochemical basis of yellow feather pigmentation in budgerigars. Cell 171, 427–439.e21 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Nisar, N., Li, L., Lu, S., Khin, N. C. & Pogson, B. J. Carotenoid metabolism in plants. Mol. Plant. 8, 68–82 (2015).

    CAS  PubMed  Google Scholar 

  11. Moran, N. A. & Jarvik, T. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328, 624–627 (2010).

    CAS  PubMed  Google Scholar 

  12. Lopes, R. J. et al. Genetic basis for red coloration in birds. Curr. Biol. 26, 1427–1434 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Mundy, N. I. I. et al. Red carotenoid coloration in the zebra finch is controlled by a cytochrome P450 gene cluster. Curr. Biol. 26, 1435–1440 (2016).

    CAS  PubMed  Google Scholar 

  14. Hébant, C. & Lee, D. W. Ultrastructural basis and developmental control of blue iridescence in Selaginella leaves. Am. J. Botany 71, 216–219 (1984).

    Google Scholar 

  15. Vukusic, P., Sambles, J. R., Lawrence, C. R. & Wootton, R. J. Quantified interference and diffraction in single Morpho butterfly scales. Proc. Biol. Sci. 266, 1403–1411 (1999).

    PubMed Central  Google Scholar 

  16. Vane-Wright, R. I. A unified classification of mimetic resemblances. Biol. J. Linn. Soc. 8, 25–56 (1976).

    Google Scholar 

  17. Twomey, E., Vestergaard, J. S., Venegas, P. J. & Summers, K. Mimetic divergence and the speciation continuum in the mimic poison frog Ranitomeya imitator. Am. Nat. 187, 205–224 (2015).

    PubMed  Google Scholar 

  18. Smith, Da. S. Phenotypic diversity, mimicry and natural selection in the African butterfly Hypolimnas misippus L. (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 8, 183–204 (1976).

    Google Scholar 

  19. Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, 1930).

  20. Orr, H. A. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935–949 (1998).

    PubMed  Google Scholar 

  21. Orr, H. A. The genetic theory of adaptation: a brief history. Nat. Rev. Genet. 6, 119–127 (2005).

    CAS  PubMed  Google Scholar 

  22. Martin, A. & Courtier-Orgogozo, V. in Diversity and Evolution of Butterfly Wing Patterns: An Integrative Approach (eds. Sekimura, T. & Nijhout, H. F.) 59–87 (Springer, 2017).

  23. Martin, A. & Orgogozo, V. The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67, 1235–1250 (2013).

    CAS  PubMed  Google Scholar 

  24. Uy, J. A. C. et al. Mutations in different pigmentation genes are associated with parallel melanism in island flycatchers. Proc. Biol. Sci. 283, 20160731 (2016).

    PubMed  PubMed Central  Google Scholar 

  25. Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. & Crossland, J. P. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101–104 (2006).

    CAS  PubMed  Google Scholar 

  26. Römpler, H. et al. Nuclear gene indicates coat-color polymorphism in mammoths. Science 313, 62 (2006).

    PubMed  Google Scholar 

  27. Yuan, Y.-W., Rebocho, A. B., Sagawa, J. M., Stanley, L. E. & Bradshaw, H. D. Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species. Proc. Natl Acad. Sci. USA 113, 2448–2453 (2016). This study identifies a gene encoding an R2R3-MYB transcription factor as the causal gene underlying flower spatial pattern variation in two species of monkeyflowers with different pollinators.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Albert, N. W. et al. A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant. Cell 26, 962–980 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Kellenberger, R. T. et al. Emergence of a floral colour polymorphism by pollinator-mediated overdominance. Nat. Commun. 10, 63 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Toomey, M. B. et al. High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds. Proc. Natl Acad. Sci. USA 114, 5219–5224 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. van’t Hof, A. E. et al. The industrial melanism mutation in British peppered moths is a transposable element. Nature 534, 102–105 (2016).

    PubMed  Google Scholar 

  32. Nadeau, N. J. et al. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature 534, 106–110 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Reed, R. D. et al. Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333, 1137–1141 (2011).

    CAS  PubMed  Google Scholar 

  34. Mazo-Vargas, A. et al. Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity. Proc. Natl Acad. Sci. USA 114, 10701–10706 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Westerman, E. L. et al. Aristaless controls butterfly wing color variation used in mimicry and mate choice. Curr. Biol. 28, 3469–3474.e4 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Kratochwil, C. F. et al. Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations. Science 362, 457–460 (2018). This article describes an example of phenotypic convergence through independent mutations at the same locus. Different cis-regulatory mutations near the gene encoding agouti-related peptide 2 lower its expression and produce convergent striped phenotypes in cichlid fish.

    CAS  PubMed  Google Scholar 

  37. Zhang, C. et al. Pineal-specific agouti protein regulates teleost background adaptation. Proc. Natl Acad. Sci. USA 107, 20164–20171 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Küpper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 79–83 (2015). This article, together with reference 39, shows that a complex phenotype encompassing differences in body size, ornamentation and aggressive and mating behaviour in the ruff is controlled by a supergene containing an inversion.

    PubMed  PubMed Central  Google Scholar 

  39. Lamichhaney, S. et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48, 84–88 (2016).

    CAS  PubMed  Google Scholar 

  40. Widemo, F. Alternative reproductive strategies in the ruff, Philomachus pugnax: a mixed ESS? Anim. Behav. 56, 329–336 (1998).

    CAS  PubMed  Google Scholar 

  41. Thompson, M. J. & Jiggins, C. D. Supergenes and their role in evolution. Heredity 113, 1–8 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Iijima, T. et al. Parallel evolution of Batesian mimicry supergene in two Papilio butterflies, P. polytes and P. memnon. Sci. Adv. 4, eaao5416 (2018).

    PubMed  PubMed Central  Google Scholar 

  43. Kunte, K. et al. Doublesex is a mimicry supergene. Nature 507, 229–232 (2014).

    CAS  PubMed  Google Scholar 

  44. Nishikawa, H. et al. A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly. Nat. Genet. 47, 405–409 (2015).

    CAS  PubMed  Google Scholar 

  45. Graham, S. M., Watt, W. B. & Gall, L. F. Metabolic resource allocation vs. mating attractiveness: adaptive pressures on the “alba” polymorphism of Colias butterflies. Proc. Natl Acad. Sci. USA 77, 3615–3619 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Woronik, A. et al. A transposable element insertion is associated with an alternative life history strategy. Nat. Commun. 10, 1–11 (2019).

    Google Scholar 

  47. Toomey, M. B. et al. A non-coding region near Follistatin controls head colour polymorphism in the Gouldian finch. Proc. Biol. Sci. 285, 20181788 (2018).

    PubMed  PubMed Central  Google Scholar 

  48. Kim, K.-W. et al. Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird. Nat. Commun. 10, 1852 (2019).

    PubMed  PubMed Central  Google Scholar 

  49. Lehtonen, P. K. et al. Candidate genes for colour and vision exhibit signals of selection across the pied flycatcher (Ficedula hypoleuca) breeding range. Heredity 108, 431–440 (2012).

    CAS  PubMed  Google Scholar 

  50. Toews, D. P. L. et al. Plumage genes and little else distinguish the genomes of hybridizing warblers. Curr. Biol. 26, 2313–2318 (2016).

    CAS  PubMed  Google Scholar 

  51. Hopkins, R. & Rausher, M. D. Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469, 411–414 (2011).

    CAS  PubMed  Google Scholar 

  52. Hopkins, R. & Rausher, M. D. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335, 1090–1092 (2012).

    CAS  PubMed  Google Scholar 

  53. Schwander, T., Libbrecht, R. & Keller, L. Supergenes and complex phenotypes. Curr. Biol. 24, R288–R294 (2014).

    CAS  PubMed  Google Scholar 

  54. Ford, E. B. Genetic Polymorphism (Faber & Faber, 1965).

  55. Turner, J. R. G. On supergenes. I. The evolution of supergenes. Am. Nat. 101, 195–221 (1967).

    Google Scholar 

  56. Martin, S. H. et al. Whole-chromosome hitchhiking driven by a male-killing endosymbiont. PLoS Biol. 18, e3000610 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Joron, M. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Tuttle, E. M. et al. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol. 26, 344–350 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Muller, H. J. Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics 3, 422–499 (1918).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Jay, P. et al. Mutation accumulation in chromosomal inversions maintains wing pattern polymorphism in a butterfly. Preprint at bioRxiv https://doi.org/10.1101/736504 (2019).

    Article  Google Scholar 

  61. Papa, R. et al. Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in heliconius erato. PLoS One 8, e57033 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Dembeck, L. M. et al. Genetic architecture of abdominal pigmentation in drosophila melanogaster. PLoS Genet. 11, e1005163 (2015).

    PubMed  PubMed Central  Google Scholar 

  63. Brien Melanie, N. et al. Phenotypic variation in Heliconius erato crosses shows that iridescent structural colour is sex-linked and controlled by multiple genes. Interface Focus 9, 20180047 (2019).

    CAS  PubMed  Google Scholar 

  64. Morgan, M. D. et al. Genome-wide study of hair colour in UK Biobank explains most of the SNP heritability. Nat. Commun. 9, 1–10 (2018).

    Google Scholar 

  65. Hysi, P. G. et al. Genome-wide association meta-analysis of individuals of European ancestry identifies new loci explaining a substantial fraction of hair color variation and heritability. Nat. Genet. 50, 652–656 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Carroll, S. B., Grenier, J. K. & Weatherbee, S. D. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design 2nd edn (Blackwell, 2005).

  67. Rebeiz, M., Pool, J. E., Kassner, V. A., Aquadro, C. F. & Carroll, S. B. Stepwise modification of a modular enhancer underlies adaptation in a drosophila population. Science 326, 1663–1667 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Massey, J. H. & Wittkopp, P. J. in Current Topics in Developmental Biology Vol. 119 (Orgogozo, V.) 27–61 (Elsevier, 2016).

  69. Tian, L. et al. A homeotic shift late in development drives mimetic color variation in a bumble bee. Proc. Natl Acad. Sci. USA 116, 11857–11865 (2019). By analysing convergent colour phenotypes in bumblebees, this study demonstrates how shifts in spatial and temporal expression can reduce pleiotropy such that a crucial developmental Hox gene can play a role in phenotypic diversification.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Seimiya, M. & Gehring, W. J. The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 127, 1879–1886 (2000).

    CAS  PubMed  Google Scholar 

  71. Jory, A. et al. A survey of 6,300 genomic fragments for cis-regulatory activity in the imaginal discs of Drosophila melanogaster. Cell Rep. 2, 1014–1024 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Lewis, J. J. et al. Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry. Proc. Natl Acad. Sci. USA 116, 24174–24183 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Rogers, W. A. et al. Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity. PLoS Genet. 9, e1003740 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Paaby, A. B. & Rockman, M. V. The many faces of pleiotropy. Trends Genet. 29, 66–73 (2013).

    CAS  PubMed  Google Scholar 

  75. Saenko, S. V. et al. Amelanism in the corn snake is associated with the insertion of an LTR-retrotransposon in the OCA2 gene. Sci. Rep. 5, 17118 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Johanson, H. C., Chen, W., Wicking, C. & Sturm, R. A. Inheritance of a novel mutated allele of the OCA2 gene associated with high incidence of oculocutaneous albinism in a Polynesian community. J. Hum. Genet. 55, 103–111 (2010).

    PubMed  Google Scholar 

  77. Crawford, N. G. et al. Loci associated with skin pigmentation identified in African populations. Science 358, eaan8433 (2017).

    PubMed  PubMed Central  Google Scholar 

  78. Bilandžija, H., Ma, L., Parkhurst, A. & Jeffery, W. R. A potential benefit of albinism in astyanax cavefish: downregulation of the oca2 gene increases tyrosine and catecholamine levels as an alternative to melanin synthesis. PLoS One 8, e80823 (2013).

    PubMed  PubMed Central  Google Scholar 

  79. Linnen, C. R. et al. Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339, 1312–1316 (2013).

    CAS  PubMed  Google Scholar 

  80. Linnen, C. R., Kingsley, E. P., Jensen, J. D. & Hoekstra, H. E. On the origin and spread of an adaptive allele in deer mice. Science 325, 1095–1098 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Rosenblum, E. B., Rompler, H., Schoneberg, T. & Hoekstra, H. E. Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc. Natl Acad. Sci. USA 107, 2113–2117 (2009).

    PubMed  PubMed Central  Google Scholar 

  82. Martin, A. et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc. Natl Acad. Sci. USA 109, 12632–12637 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Stern, D. L. & Orgogozo, V. Is genetic evolution predictable? Science 323, 746–751 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Tanaka, S., Harano, K., Nishide, Y. & Sugahara, R. The mechanism controlling phenotypic plasticity of body color in the desert locust: some recent progress. Curr. Opin. Insect Sci. 17, 10–15 (2016).

    PubMed  Google Scholar 

  85. Järvi, V. V., Burg van der, K. R. L. & Reed, R. D. Seasonal plasticity in Junonia coenia (Nymphalidae): linking wing color, temperature dynamics, behavior. J. Lepid. Soc. 3, 34–42 (2019).

    Google Scholar 

  86. Jones, M. R. et al. Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science 360, 1355–1358 (2018). This article describes the genetic basis of seasonal phenotypic plasticity of coat colour in snowshoe hares.

    CAS  PubMed  Google Scholar 

  87. Gibert, J.-M., Mouchel-Vielh, E., De Castro, S. & Peronnet, F. Phenotypic plasticity through transcriptional regulation of the evolutionary hotspot gene tan in Drosophila melanogaster. PLoS Genet. 12, e1006218 (2016).

    PubMed  PubMed Central  Google Scholar 

  88. Castro, S. D., Peronnet, F., Gilles, J.-F., Mouchel-Vielh, E. & Gibert, J.-M. bric à brac (bab), a central player in the gene regulatory network that mediates thermal plasticity of pigmentation in Drosophila melanogaster. PLoS Genet. 14, e1007573 (2018).

    PubMed  PubMed Central  Google Scholar 

  89. Corl, A. et al. the genetic basis of adaptation following plastic changes in coloration in a novel environment. Curr. Biol. 28, 2970–2977.e7 (2018).

    CAS  PubMed  Google Scholar 

  90. Ando, T. et al. Repeated inversions within a pannier intron drive diversification of intraspecific colour patterns of ladybird beetles. Nat. Commun. 9, 3843 (2018).

    PubMed  PubMed Central  Google Scholar 

  91. Gautier, M. et al. The genomic basis of color pattern polymorphism in the harlequin ladybird. Curr. Biol. 28, 3296–3302.e7 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Giska, I. et al. Introgression drives repeated evolution of winter coat color polymorphism in hares. Proc. Natl Acad. Sci. USA 116, 24150–24156 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Anderson, T. M. et al. Molecular and evolutionary history of melanism in north american gray wolves. Science 323, 1339–1343 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Wallbank, R. W. R. et al. Evolutionary novelty in a butterfly wing pattern through enhancer shuffling. PLoS Biol. 14, e1002353 (2016). This study shows that shuffling of two narrow enhancer regions between Heliconius species has led to phenotype diversification, exemplifying the importance of introgression in morphological innovation.

    PubMed  PubMed Central  Google Scholar 

  95. Marques, D. A., Meier, J. I. & Seehausen, O. A combinatorial view on speciation and adaptive radiation. Trends Ecol. Evol. 34, 531–544 (2019).

    PubMed  Google Scholar 

  96. Barrett, R. D. H. et al. Linking a mutation to survival in wild mice. Science 363, 499–504 (2019).

    CAS  PubMed  Google Scholar 

  97. Nosil, P. et al. Natural selection and the predictability of evolution in Timema stick insects. Science 359, 765–770 (2018).

    CAS  PubMed  Google Scholar 

  98. Moest, M. et al. Selective sweeps on novel and introgressed variation shape mimicry loci in a butterfly adaptive radiation. PLoS Biol. 18, e3000597 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Mallet, J. & Barton, N. H. Strong natural selection in a warning-color hybrid zone. Evolution 43, 421–431 (1989).

    PubMed  Google Scholar 

  100. Kapan, D. D. Three-butterfly system provides a field test of müllerian mimicry. Nature 409, 338–340 (2001).

    CAS  PubMed  Google Scholar 

  101. Matsuoka, Y. & Monteiro, A. Melanin pathway genes regulate color and morphology of butterfly wing scales. Cell Rep. 24, 56–65 (2018).

    CAS  PubMed  Google Scholar 

  102. Jiggins, C. D. A flamboyant behavioral polymorphism is controlled by a lethal supergene. Nat. Genet. 48, 7–8 (2016).

    CAS  PubMed  Google Scholar 

  103. Rice, E. S. & Green, R. E. New approaches for genome assembly and scaffolding. Annu. Rev. Anim. Biosci. 7, 17–40 (2019).

    CAS  PubMed  Google Scholar 

  104. Pardo-Diaz, C., Salazar, C. & Jiggins, C. D. Towards the identification of the loci of adaptive evolution. Methods Ecol. Evol. 6, 445–464 (2015).

    PubMed  PubMed Central  Google Scholar 

  105. Liu, B. H. Statistical Genomics: Linkage, Mapping, and QTL Analysis (CRC, 1997).

  106. Pickar-Oliver, A. & Gersbach, C. A. The next generation of CRISPR–Cas technologies and applications. Nat. Rev. Mol. Cell Biol. 20, 490–507 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Wilson, R. C. & Doudna, J. A. Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 42, 217–239 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank everyone at the Butterfly Genetics Group at the University of Cambridge for useful discussion and comments on the manuscript. A.O. was supported by a UK Natural Environment Research Council doctoral training partnership (grant NE/L002507/1) and C.D.J. was supported by a European Research Council (grant 339873 Speciation Genetics) and UK Biotechnology and Biological Sciences Research Council grant BB/R007500/1.

Author information

Authors and Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding authors

Correspondence to Anna Orteu or Chris D. Jiggins.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Genetics thanks M. Carneiro, I. Saccheri and C. Wheat for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Association studies

Studies that correlate phenotypic variation with genetic variation. The most common methods are genome-wide association studies and quantitative trait locus mapping studies.

Polymorphism

The occurrence of two or more distinct phenotypes or morphs of a species within a population.

Genetic architecture

The genetic basis underlying variation in a phenotypic trait. The main characteristics are the number of loci, their interactions and effect sizes, and their relative positions in the genome.

Quantitative trait loci

Genomic regions at which there is a correlation between genetic variation and phenotypic variation in a trait of interest among individuals from a laboratory-generated cross.

Heterozygote advantage

A scenario in which the heterozygous genotype is fitter than either homozygous genotype.

Transposable element

A genetic element that can move from one position in the genome to another.

cis-regulatory element

(CRE). A genetic region that regulates expression of a coding sequence on the same DNA strand.

Selection coefficient

A measure of the difference in fitness between two genotypes, which are a necessary condition for the action of natural selection.

Negative frequency-dependent selection

An evolutionary process in which the fitness of a genotype or phenotype depends on its frequency in the population relative to other genotypes or phenotypes such that its fitness decreases as its frequency increases.

Purifying selection

The selective removal of deleterious alleles from the population.

Effective population size

The number of individuals in an idealized population that would show the same degree of genetic drift as seen in the real population.

Polygenic inheritance

Also known as polygenicity. The genetic control of a phenotype by multiple genes of small effect.

Genome-wide association study

(GWAS). A study that correlates genetic variation between individuals across the genome with phenotypic variation among those same individuals, typically in a wild population. Associated regions are inferred to contain causal variants controlling phenotypic variation. More generally known as ‘association studies’.

Stabilizing selection

A selective force that maintains the population phenotypic mean and eliminates extreme values.

Convergence

The independent evolution of similar features in different lineages or species.

Pleiotropy

The effect of a single mutation on multiple aspects of the phenotype.

‘Input–output’ genes

Genes that integrate complex spatiotemporal information and trigger alternative developmental outputs.

Phenotypic plasticity

The ability of a single genotype to produce a range of phenotypes depending on the environmental conditions.

Polyphenism

A type of phenotypic plasticity in which a single genotype can produce two or more discrete alternative phenotypes depending on the environmental conditions.

Reaction norms

Patterns of phenotypic expression of a single genotype across differing environmental conditions.

Balancing selection

Selective processes that maintain multiple alleles in a population, such as negative frequency-dependent selection and heterozygote advantage.

Introgression

The transfer of genetic material from one species to another through hybridization.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orteu, A., Jiggins, C.D. The genomics of coloration provides insights into adaptive evolution. Nat Rev Genet 21, 461–475 (2020). https://doi.org/10.1038/s41576-020-0234-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41576-020-0234-z

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing