Sexual selection and genetic colour polymorphisms in animals

Molecular Ecology

Volumn 23, Issue 22, 2014, Pages 5398-5414

  Wellenreuther, Maren ^a   Svensson, Erik I ^a   Hansson, Bengt ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

adaptive introgression; colour polymorphisms; frequency dependent selection; inversions; linkage; mate choice; recombination; sexual selection; supergenes

Indexed keywords

ANIMALIA;

ANIMAL; EVOLUTION; FEMALE; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; MALE; MATE CHOICE; PIGMENTATION;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; GENETIC LINKAGE; MALE; MATING PREFERENCE, ANIMAL; PIGMENTATION; POLYMORPHISM, GENETIC; SELECTION, GENETIC;

EID: 84920822914     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12935     Document Type: Review

References (102)

1. Abbott J, Svensson EI, (2005) Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly. Journal of Evolutionary Biology, 18, 1464-1470.
2. Albertson RC, Streelman JT, Kocher TD, Yelick PC, (2005) Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences of the United States of America, 102, 16287-16292.
3. Barlow GW, (1973) Competition between color morphs of the polychromatic Midas cichlid Cichlasoma citrinellum. Science, 179, 806-807.
4. Barlow G, (1983) The benefits of being gold: behavioral consequences of polychromatism in the midas cichlid, Cichlasoma citrinellum. Environmental Biology of Fishes, 8, 235-247.
5. Barluenga M, Meyer A, (2004) Mechanisms of speciation in the highly polymorphic Midas cichlid species complex. Molecular Ecology, 13, 2061-2076.
6. Bleay C, Sinervo B, (2007) Discrete genetic variation in mate choice and a condition-dependent preference function in the side-blotched lizard: implications for the formation and maintenance of coadapted gene complexes. Behavioral Ecology, 18, 304-310.
7. Blows MW, Brooks R, Kraft PG, (2003) Exploring complex fitness surfaces: multiple ornamentation and polymorphism in male guppies. Evolution, 57, 1622-1630.
8. Braasch I, Schartl M, Volff JN, (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evolutionary Biology, 7, 74.
9. Brodie ED III, (1989) Genetic correlations between morphology and antipredator behaviour in natural populations of the garter snake Thamnophis ordinoides. Nature, 342, 542-543.
10. Brodie ED III, (1992) Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution, 46, 1284-1298.
11. Carleton KL, Kocher TD, (2001) Cone opsin genes of african cichlid fishes: tuning spectral sensitivity by differential gene expression. Molecular Biology and Evolution, 18, 1540-1550.
12. Cheverud JM, (1984) Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155-171.
13. Clarke CA, Sheppard PM, (1972) The genetics of the mimetic butterfly Papilio polytes L. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 263, 431-458.
14. Colombo M, Diepeveen ET, Muschick M, et al,. (2013) The ecological and genetic basis of convergent thick-lipped phenotypes in cichlid fishes. Molecular Ecology, 22, 670-684.
15. Dijkstra PD, Lindstrom J, Metcalfe NB, et al,. (2010) Frequency-dependent social dominance in a color polymorphic cichlid fish. Evolution, 64, 2797-2807.
16. Fan S, Elmer KR, Meyer A, (2012) Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and neotropical lineages. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367, 385-394.
17. Fincke O, Jodicke R, Paulson D, Schultz T, (2005) The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like females typically the minority? International Journal of Odonatology, 8, 183-212.
18. Ford EB, (1945) Polymorphism. Biological Reviews and Biological Proceedings of the Cambridge Philosophical Society, 20, 73-88.
19. Forsman A, (2013) Effects of genotypic and phenotypic variation on establishment are important for conservation, invasion, and infection biology. Proceedings of the National Academy of Sciences of the United States of America, 111, 302-307.
20. Forsman A, Ahnesjö J, Caesar S, Karlsson M, (2008) A model of ecological and evolutionary consequences of color polymoprhism. Ecology, 89, 34-40.
21. Galeotti P, Rubolini D, Dunn PO, Fasola M, (2003) Colour polymorphism in birds: causes and functions. Journal of Evolutionary Biology, 16, 635-646.
22. Gavrilets S, (2004) Fitness Landscapes and the Origin of Species, 1st edn. Princeton University Press, Princeton, New Jersey.
23. Gosden TP, Svensson EI, (2008) Spatial and temporal dynamics in a geographic sexual selection mosaic. Evolution, 62, 845-856.
24. Gosden T, Svensson E, (2009) Density-dependent male mating harassment, female resistance, and male mimicry. The American Naturalist, 173, 709-721.
25. Gratten J, Wilson AJ, McRae AF, et al,. (2008) A localized negative genetic correlation constrains microevolution of coat color in wild sheep. Science, 319, 318-320.
26. Gray SM, Dill LM, Tantu FY, et al,. (2008) Environment-contingent sexual selection in a colour polymorphic fish. Proceedings of the Royal Society of London B: Biological Sciences, 275, 1785-1791.
27. Hendry AP, Troy D, (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology, 14, 901-916.
28. Henning F, Renz AJ, Fukamachi S, Meyer A, (2010) Genetic, comparative genomic, and expression analyses of the Mc1r locus in the polychromatic Midas cichlid fish (Teleostei, Cichlidae Amphilophus sp.) species group. Journal of Molecular Evolution, 70, 405-412.
29. Hoekstra HE, (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity, 97, 222-234.
30. Hofreiter M, Schöneberg T, (2010) The genetic and evolutionary basis of colour variation in vertebrates. Cellular and Molecular Life Sciences, 67, 2591-2603.
31. Hugall AF, Stuart-Fox D, (2012) Accelerated speciation in colour-polymorphic birds. Nature, 485, 631-634.
32. Hughes KA, Houde AE, Price AC, Rodd FH, (2013) Mating advantage for rare males in wild guppy populations. Nature, 503, 108-110.
33. Huxley JS, (1955) Morphism and evolution. Heredity, 9, 1-52.
34. Huynh LY, Maney DL, Thomas JW, (2011) Chromosome-wide linkage disequilibrium caused by an inversion polymorphism in the white-throated sparrow (Zonotrichia albicollis). Heredity, 106, 537-546.
35. Iserbyt A, Bots J, Van Gossum H, Sherratt T, (2013) Negative frequency-dependent selection or alternative reproductive tactics: maintenance of female polymorphism in natural populations. BMC Evolutionary Biology, 13, 139.
36. Johnston SE, Gratten J, Berenos C, et al,. (2013) Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature, 502, 93-95.
37. Jones RT, Salazar PA, Ffrench-Constant RH, Jiggins CD, Joron M, (2011) Evolution of a mimicry supergene from a multilocus architecture. Proceedings of the Royal Society of London B: Biological Sciences, 279, 316-325.
38. Joron M, Papa R, Beltrán M, et al,. (2006) A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biology, 4, e303.
39. Joron M, Frezal L, Jones RT, et al,. (2011) Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature, 477, 203-206.
40. Kettlewell HBD, (1961) The phenomenon of industrial melanism in Lepidoptera. Annual Review of Entomology, 6, 245-262.
41. Kirkpatrick M, Nuismer SL, (2004) Sexual selection can constrain sympatric speciation. Proceedings of the Royal Society of London B: Biological Sciences, 271, 687-693.
42. Kocher T, (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics, 5, 288-298.
43. Kopp M, Hermisson J, (2006) The evolution of genetic architecture under frequency-dependent disruptive selection. Evolution, 60, 1537-1550.
44. Kronforst M, Young L, Kapan D, et al,. (2006) Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proceedings of the National Academy of Sciences of the United States of America, 103, 6575-6580.
45. Krüger O, Lindström J, Amos W, (2001) Maladaptive mate choice maintained by heterozygote advantage. Evolution, 55, 1207-1214.
46. Kunte K, Zhang W, Tenger-Trolander A, et al,. (2014) Doublesex is a mimicry supergene. Nature, 507, 229-232.
47. Lande R, Seehausen O, Van Alphen JJM, (2001) Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica, 112-113, 435-443.
48. Lank DB, Smith CM, Hanotte O, Burke T, Cooke F, (1995) Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature, 378, 59-62.
49. Levene H, (1953) Genetic equilibrium when more than one ecological niche is available. The American Naturalist, 87, 331-333.
50. Linnen CR, Kingsley EP, Jensen JD, Hoekstra HE, (2009) On the origin and spread of an adaptive allele in deer mice. Science, 325, 1095-1098.
51. Lucas Lledõ JI, Cáceres M, (2013) On the power and the systematic biases of the detection of chromosomal inversions by paired-end genome sequencing. PLoS ONE, 8, e61292.
52. Maan ME, Cummings ME, (2009) Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proceedings of the National Academy of Sciences of the United States of America, 106, 19072-19077.
53. Maan ME, Cummings ME, (2012) Poison frog colors are honest signals of toxicity, particularly for bird predators. The American Naturalist, 179, E1-E14.
54. Maan ME, Seehausen O, (2011) Ecology, sexual selection and speciation. Ecology Letters, 14, 591-602.
55. Maan ME, Sefc KM, (2013) Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. Seminars in Cell & Developmental Biology, 24, 516-528.
56. Magalhaes IS, Mwaiko S, Seehausen O, (2010) Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria. Molecular Ecology, 19, 3285-3300.
57. Mallet J, (1989) The Genetics of Warning Colour in Peruvian Hybrid Zones of Heliconius erato and H. melpomene. Proceedings of the Royal Society of London. B. Biological Sciences, 236, 163-185.
58. Martin A, Papa R, Nadeau NJ, et al,. (2012) Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proceedings of the National Academy of Sciences of the United States of America, 109, 12632-12637.
59. Mattersdorfer K, Koblmuller S, Sefc KM, (2012) AFLP genome scans suggest divergent selection on colour patterning in allopatric colour morphs of a cichlid fish. Molecular Ecology, 21, 3531-3544.
60. McKinnon JS, Pierotti MER, (2010) Colour polymorphism and correlated characters: genetic mechanisms and evolution. Molecular Ecology, 19, 5101-5125.
61. Mundy NI, Badcock NS, Hart T, et al,. (2004) Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science, 303, 1870-1873.
62. Nadeau NJ, Whibley A, Jones RT, et al,. (2012) Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367, 343-353.
63. Naisbit RE, Jiggins CD, Mallet J, (2001) Disruptive sexual selection against hybrids contributes to speciation between Heliconus cydno and Heliconus melpomene. Proceedings of the Royal Society of London B: Biological Sciences, 268, 1-6.
64. Naisbit RE, Jiggins CD, Mallet J, (2003) Mimicry: developmental genes that contribute to speciation. Evol Dev, 5, 269-280.
65. Olendorf R, Rodd FH, Punzalan D, et al,. (2006) Frequency-dependent survival in natural guppy populations. Nature, 441, 633-636.
66. Pardo-Diaz C, Salazar C, Baxter SW, et al,. (2012) Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genetics, 8, e1002752.
67. Pierotti MER, Martín-Fernández JA, Seehausen O, (2009) Mapping individual variation in male mating preference space: multiple choice in a color polymorphic cichlid fish. Evolution, 63, 2372-2388.
68. Plaistow SJ, Tsubaki Y, (2000) A selective trade-off for territoriality and non-territoriality in the polymorphic damselfly Mnais costalis. Proceedings of the Royal Society of London B: Biological Sciences, 267, 969-975.
69. Pryke SR, (2010) Sex chromosome linkage of mate preference and color signal maintains assortative mating between interbreeding finch morphs. Evolution, 64, 1301-1310.
70. Pryke SR, Griffith SC, (2006) Red dominates black: agonistic signalling among head morphs in the colour polymorphic Gouldian finch. Proceedings of the Royal Society of London B: Biological Sciences, 273, 949-957.
71. Pryke SR, Astheimer LB, Buttemer WA, Griffith SC, (2007) Frequency-dependent physiological trade-offs between competing colour morphs. Biology Letters, 3, 494-497.
72. Qvarnstrom A, Bailey RI, (2008) Speciation through evolution of sex-linked genes. Heredity, 102, 4-15.
73. Reed RD, Papa R, Martin A, et al,. (2011) Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science, 333, 1137-1141.
74. Roberts RB, Ser JR, Kocher TD, (2009) Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science, 326, 998-1001.
75. Roff DA, Fairbairn DJ, (2012) A test of the hypothesis that correlational selection generates genetic correlations. Evolution, 66, 2953-2960.
76. Rosenthal MF, Murphy TG, Darling N, Tarvin KA, (2012) Ornamental bill color rapidly signals changing condition. Journal of Avian Biology, 43, 553-564.
77. Roulin A, (2004) The evolution, maintenance and adaptative function of genetic colour polymorphism in birds. Biological Reviews, 79, 815-848.
78. Roulin A, Ducrest AL, (2013) Genetics of colouration in birds. Seminars in Cell & Developmental Biology, 24, 594-608.
79. Rueffler C, Van Dooren TJM, Leimar O, Abrams PA, (2006) Disruptive selection and then what? Trends in Ecology & Evolution, 21, 238-245.
80. Sánchez-Guillén RA, Van Gossum H, Cordero-Rivera A, (2005) Hybridization and the inheritance of female colour polymorphism in two Ischnurid damselflies (Odonata: Coenagrionidae). Biological Journal of the Linnean Society, 85, 471-481.
81. Sánchez-Guillén R, Hansson B, Wellenreuther M, Svensson E, Cordero-Rivera A, (2011a) The influence of stochastic and selective forces in the population divergence of female colour polymorphism in damselflies of the genus Ischnura. Heredity, 107, 513-522.
82. Sánchez-Guillén RA, Wellenreuther M, Cordero-Rivera A, Hansson B, (2011b) Introgression and rapid species turnover in sympatric damselflies. BMC Evolutionary Biology, 11, 210.
83. Sánchez-Guillén RA, Wellenreuther M, Cordero-Rivera AS, (2012) Strong asymmetry in the relative strengths of prezygotic and postzygotic barriers between two damselfly sister species. Evolution, 66, 690-707.
84. Sánchez-Guillén RA, Cõrdoba-Aguilar A, Cordero-Rivera AS, Wellenreuther M, (2013a) Genetic divergence predicts reproductive isolation in damselflies. Journal of Evolutionary Biology, 27, 76-87.
85. Sánchez-Guillén RA, Hammers M, Hansson B, et al,. (2013b) Ontogenetic shifts in male mating preference and morph-specific polyandry in a female colour polymorphic insect. BMC Evolutionary Biology, 13. Available from http://www.biomedcentral.com/1471-2148/13/116.
86. Santos ME, Salzburger W, (2012) How cichlids diversify. Science, 338, 619-621.
87. Schwander T, Libbrecht R, Keller L, (2014) Supergenes and complex phenotypes. Current Biology, 24, 288-294.
88. Seehausen O, Mayhew PJ, Van Alphen JJM, (1999a) Evolution of colour patterns in East African cichlid fish. Journal of Evolutionary Biology, 12, 514-534.
89. Seehausen O, Van Alphen JJM, Lande R, (1999b) Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection. Ecology Letters, 2, 367-378.
90. Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P, (2011) Magic traits in speciation: 'magic' but not rare? Trends in Ecology and Evolution, 26, 389-397.
91. Sinervo B, Lively CM, (1996) The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240-243.
92. Sinervo B, Svensson E, (2002) Correlational selection and the evolution of genomic architecture. Heredity, 89, 329-338.
93. Snowberg LK, Bolnick DI, (2012) Partitioning the effects of spatial isolation, nest habitat, and individual diet in causing assortative mating within a population of threespine stickleback. Evolution, 66, 3582-3594.
94. Streelman JT, Albertson RC, Kocher TD, (2003) Genome mapping of the orange blotch colour pattern in cichlid fishes. Molecular Ecology, 12, 2465-2471.
95. Summers K, Symula R, Clough M, Cronin T, (1999) Visual mate choice in poison frogs. Proceedings of the Royal Society of London B: Biological Sciences, 266, 2141-2145.
96. Svensson E, Abbott J, Hardling R, (2005) Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations. The American Naturalist, 165, 567-576.
97. Svensson E, Abbott J, Gosden T, Coreau A, (2009) Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evolutionary Ecology, 23, 93-108.
98. Takahashi Y, Watanabe M, (2010) Female reproductive success is affected by selective male harassment in the damselfly Ischnura senegalensis. Animal Behaviour, 79, 211-216.
99. Tezuka A, Yamamoto H, Yokoyama J, van Oosterhout C, Kawata M, (2011) The MC1R gene in the guppy (Poecilia reticulata): genotypic and phenotypic polymorphisms. BMC Research Notes, 4, 31.
100. Tuttle EM, (2003) Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence. Behavioral Ecology, 14, 425-432.
101. Van Gossum H, Sherratt TN, Cordero-Rivera A, C¢rdoba-Aguilar A, (2008) The evolution of sex-limited colour polymorphism. In: Dragonflies & Damselflies. Model Organisms for Ecological and Evolutionary Research (ed., Cordoba-Aguilar A,), pp. 219-229. Oxford University Press, Oxford, UK.
102. Wagner GP, Altenberg L, (1996) Perspective: complex adaptations and the evolution of evolvability. Evolution, 50, 967-976.