1932

Abstract

The evolution of female ornamentation has been subject to considerable debate. Although originally thought to be by-products of selection on males, recent studies have emphasized the adaptive nature of female ornaments. Here, I review current knowledge on the genetic architecture of ornamental traits and how their expression is (or is not) restricted to one sex. Ornament development typically involves deeply conserved developmental genes. Their expression is modified by pre-existing sexually dimorphic signals, such as hormones in vertebrates or gene products in insects. Changes in dosage and binding affinities in these systems apparently allow frequent switches between sexually dimorphic and monomorphic ornament expression. However, early-developing ornaments may be difficult to modulate, as this would result in severe pleiotropic effects. Comparative studies on the molecular structure of the sex-specific modulating signals and their receptors should provide detailed insight into the mechanisms underlying the loss and gain of female ornaments.

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2014-11-23
2024-12-02
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Literature Cited

  1. Al-khairulla H, Warburton D, Knell RJ. 2003. Do the eyestalks of female diopsid flies have a function in intrasexual aggressive encounters?. J. Insect Behav. 16:5679–86 [Google Scholar]
  2. Amundsen T. 2000. Why are female birds ornamented?. Trends Ecol. Evol. 15:4149–55 [Google Scholar]
  3. Andersson M. 1994. Sexual Selection Princeton, NJ: Princeton Univ. Press [Google Scholar]
  4. Baker RH, Narechania A, Johns PM, Wilkinson GS. 2012. Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae). Philos. Trans. R. Soc. Lond. B.-Biol. Sci. 367:16002357–75 [Google Scholar]
  5. Baker RH, Wilkinson GS. 2001. Phylogenetic analysis of sexual dimorphism and eye-span allometry in stalk-eyed flies (Diopsidae). Evolution 55:71373–85 [Google Scholar]
  6. Baker RH, Wilkinson GS. 2010. Comparative genomic hybridization (CGH) reveals a neo-X chromosome and biased gene movement in stalk-eyed flies (genus Teleopsis). PLOS Genet. 6:9e1001121 [Google Scholar]
  7. Boije H, Harun-Or-Rashid M, Lee Y-J, Imsland F, Bruneau N. et al. 2012. Sonic hedgehog-signalling patterns the developing chicken comb as revealed by exploration of the Pea-comb mutation. PLOS ONE 7:12e50890 [Google Scholar]
  8. Bond CW, Angeloni NL, Podlasek CA. 2010. Analysis of testosterone effects on sonic hedgehog signaling in juvenile, adolescent and adult Sprague Dawley rat penis. J. Sex. Med. 7:31116–25 [Google Scholar]
  9. Cardoso GC, Mota PG. 2010. Evolution of female carotenoid coloration by sexual constraint in Carduelis finches. BMC Evol. Biol. 10:82 [Google Scholar]
  10. Cho S, Wensink PC. 1997. DNA binding by the male and female doublesex proteins of Drosophila melanogaster. J. Biol. Chem. 272:63185–89 [Google Scholar]
  11. Clutton-Brock T. 2009. Sexual selection in females. Anim. Behav. 77:13–11 [Google Scholar]
  12. Devi TR, Shyamala B. 2013. Male- and female-specific variants of doublesex gene products have different roles to play towards regulation of Sex combs reduced expression and sex comb morphogenesis in Drosophila. J. Biosci. 38:3455–60 [Google Scholar]
  13. Doane RW. 1913. How Oryctes rhinoceros, a dynastid beetle, uses its horn. Science 38:990883 [Google Scholar]
  14. Drouin G, Godin J-R, Pagé B. 2011. The genetics of vitamin C loss in vertebrates. Curr. Genomics 12:5371–78 [Google Scholar]
  15. Eaton MD. 2006. A phylogenetic perspective on the evolution of chromatic ultraviolet plumage coloration in grackles and allies (Icteridae). Auk 123:1211–34 [Google Scholar]
  16. Emlen DJ, Marangelo J, Ball B, Cunningham CW. 2005. Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:51060–84 [Google Scholar]
  17. Gould SJ. 1970. Dollo on Dollo's law: irreversibility and the status of evolutionary laws. J. Hist. Biol. 3:2189–212 [Google Scholar]
  18. Hingle A, Fowler K, Pomiankowski A. 2001. Size-dependent mate preference in the stalk-eyed fly Cyrtodiopsis dalmanni. Anim. Behav. 61:3589–95 [Google Scholar]
  19. Hofmann CM, Cronin TW, Omland KE. 2008. Evolution of sexual dichromatism. 1. Convergent losses of elaborate female coloration in new world orioles (Icterus spp.). Auk 125:4778–89 [Google Scholar]
  20. Horton BM, Hudson WH, Ortlund EA, Shirk S, Thomas JW. et al. 2014. Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes. Proc. Natl. Acad. Sci. USA 111:41443–48 [Google Scholar]
  21. Imsland F, Feng C, Boije H, Bed'hom B, Fillon V. et al. 2012. The rose-comb mutation in chickens constitutes a structural rearrangement causing both altered comb morphology and defective sperm motility. PLOS Genet. 8:6e1002775 [Google Scholar]
  22. Ito Y, Harigai A, Nakata M, Hosoya T, Araya K. et al. 2013. The role of doublesex in the evolution of exaggerated horns in the Japanese rhinoceros beetle. EMBO Rep. 14:6561–67 [Google Scholar]
  23. Iwasa Y, Pomiankowski A, Nee S. 1991. The evolution of costly mate preferences. II. The “handicap” principle. Evolution 45:61431–42 [Google Scholar]
  24. Jones IL, Hunter FM. 1993. Mutual sexual selection in a monogamous seabird. Nature 362:238–39 [Google Scholar]
  25. Jones IL, Hunter FM. 1999. Experimental evidence for mutual inter- and intrasexual selection favouring a crested auklet ornament. Anim. Behav. 57:3521–28 [Google Scholar]
  26. Ketterson ED, Nolan V, Sandell M. 2005. Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both?. Am. Nat. 166:S4S85–98 [Google Scholar]
  27. Khila A, Abouheif E, Rowe L. 2012. Function, developmental genetics, and fitness consequences of a sexually antagonistic trait. Science 336:6081585–89 [Google Scholar]
  28. Kijimoto T, Andrews J, Moczek AP. 2010. Programed cell death shapes the expression of horns within and between species of horned beetles. Evol. Dev. 12:5449–58 [Google Scholar]
  29. Kijimoto T, Moczek AP, Andrews J. 2012. Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns. Proc. Natl. Acad. Sci. USA 109:5020526–31 [Google Scholar]
  30. Kimball RT, Ligon JD. 1999. Evolution of avian plumage dichromatism from a proximate perspective. Am. Nat. 154:2182–93 [Google Scholar]
  31. Kimball RT, Mary CMS, Braun EL. 2011. A macroevolutionary perspective on multiple sexual traits in the Phasianidae (Galliformes). Int. J. Evol. Biol. 2011:423938 [Google Scholar]
  32. Kopp A. 2012. Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet. 28:4175–84 [Google Scholar]
  33. Kopp A, Duncan I, Carroll SB. 2000. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408:6812553–59 [Google Scholar]
  34. Kotiaho JS. 2001. Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol. Rev. Camb. Philos. Soc. 76:3365–76 [Google Scholar]
  35. Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J. 2007. The evolution of mutual ornamentation. Anim. Behav. 74:4657–77 [Google Scholar]
  36. Kraaijeveld K, Reumer BM. 2008. Constraints and the evolution of mutual ornamentation. Animal Behavior: New Research EA Weber, LH Krause 193–213 New York: Nova Sci. Publ. [Google Scholar]
  37. Labbé GMC, Scaife S, Morgan SA, Curtis ZH, Alphey L. 2012. Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus. PLOS Negl. Trop. Dis. 6:7e1724 [Google Scholar]
  38. Lahaye SEP, Eens M, Darras VM, Pinxten R. 2013. Hot or not: the effects of exogenous testosterone on female attractiveness to male conspecifics in the budgerigar. PLOS ONE 8:8e74005 [Google Scholar]
  39. Lande R. 1980. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305 [Google Scholar]
  40. Lank DB, Coupe M, Wynne-Edwards KE. 1999. Testosterone-induced male traits in female ruffs (Philomachus pugnax): autosomal inheritance and gender differentiation. Proc. R. Soc. B-Biol. Sci. 266:14352323–30 [Google Scholar]
  41. Ligon JD, Thornhill R, Zuk M, Johnson K. 1990. Male-male competition, ornamentation and the role of testosterone in sexual selection in red jungle fowl. Anim. Behav. 1942:367–73 [Google Scholar]
  42. Llopart A, Elwyn S, Coyne JA. 2002. Pigmentation and mate choice in Drosophila. Nature 419:6905360 [Google Scholar]
  43. Luo SD, Shi GW, Baker BS. 2011. Direct targets of the D. melanogaster dsxf protein and the evolution of sexual development. Development 138:132761–71 [Google Scholar]
  44. Lyon BE, Montgomerie R. 2012. Sexual selection is a form of social selection. Philos. Trans. R. Soc. Lond. B.-Biol. Sci. 367:16002266–73 [Google Scholar]
  45. McKinnell IW, Makarenkova H, de Curtis I, Turmaine M, Patel K. 2004. EphA4, RhoB and the molecular development of feather buds are maintained by the integrity of the actin cytoskeleton. Dev. Biol. 270:194–105 [Google Scholar]
  46. Mikhaylova LM, Nguyen K, Nurminsky DI. 2008. Analysis of the Drosophila melanogaster testes transcriptome reveals coordinate regulation of paralogous genes. Genetics 179:1305–15 [Google Scholar]
  47. Moczek AP, Rose DJ. 2009. Differential recruitment of limb patterning genes during development and diversification of beetle horns. Proc. Natl. Acad. Sci. USA 106:228992–97 [Google Scholar]
  48. Ord TJ, Stuart-Fox D. 2006. Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change. J. Evol. Biol. 19:3797–808 [Google Scholar]
  49. Owens IP, Short RV. 1995. Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol. Evol. 10:44–47 [Google Scholar]
  50. Panhuis TM, Wilkinson GS. 1999. Exaggerated male eye span influences contest outcome in stalk-eyed flies (Diopsidae). Behav. Ecol. Sociobiol. 46:221–27 [Google Scholar]
  51. Pfannkuche KA, Gahr M, Weites IM, Riedstra B, Wolf C, Groothuis TGG. 2011. Examining a pathway for hormone mediated maternal effects—yolk testosterone affects androgen receptor expression and endogenous testosterone production in young chicks (Gallus gallus domesticus). Gen. Comp. Endocrinol. 172:3487–93 [Google Scholar]
  52. Price JJ, Whalen LM. 2009. Plumage evolution in the oropendolas and caciques: different divergence rates in polygynous and monogamous taxa. Evolution 63:112985–98 [Google Scholar]
  53. Rice WR. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:4735–42 [Google Scholar]
  54. Riedstra B, Pfannkuche KA, Groothuis TGG. 2013. Increased exposure to yolk testosterone has feminizing effects in chickens, Gallus gallus domesticus. Anim. Behav. 85:4701–8 [Google Scholar]
  55. Robertson A, Briscoe DA, Louw JH. 1977. Variation in abdomen pigmentation in Drosophila melanogaster females. Genetica 47:173–76 [Google Scholar]
  56. Rowe L, Westlake KP, Currie DC. 2006. Functional significance of elaborate secondary sexual traits and their evolution in the water strider genus Rheumatobates. Can. Entomol. 138:568–77 [Google Scholar]
  57. Shapiro MD, Kronenberg Z, Li C, Domyan ET, Pan H. et al. 2013. Genomic diversity and evolution of the head crest in the rock pigeon. Science 339:61231063–67 [Google Scholar]
  58. Szykman M, Van Horn RC, Engh AL, Boydston EE, Holekamp KE. 2007. Courtship and mating in free-living spotted hyenas. Behaviour 144:815–46 [Google Scholar]
  59. Tanaka K, Barmina O, Kopp A. 2009. Distinct developmental mechanisms underlie the evolutionary diversification of Drosophila sex combs. Proc. Natl. Acad. Sci. USA 106:124764–69 [Google Scholar]
  60. Tobias JA, Montgomerie R, Lyon BE. 2012. The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philos. Trans. R. Soc. Lond. B.-Biol. Sci. 367:16002274–93 [Google Scholar]
  61. Valena S, Moczek AP. 2012. Epigenetic mechanisms underlying developmental plasticity in horned beetles. Genet. Res. Int. 2012:576303 [Google Scholar]
  62. Velando A, Lessells CM, Marquez JC. 2001. The function of female and male ornaments in the Inca tern: evidence for links between ornament expression and both adult condition and reproductive performance. J. Avian Biol. 32:311–18 [Google Scholar]
  63. Wasik BR, Moczek AP. 2011. Decapentaplegic (dpp) regulates the growth of a morphological novelty, beetle horns. Dev. Genes Evol. 221:117–27 [Google Scholar]
  64. Wasik BR, Rose DJ, Moczek AP. 2010. Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner. Evol. Dev. 12:4353–62 [Google Scholar]
  65. West-Eberhard MJ. 1979. Sexual selection, social competition, and evolution. Proc. Am. Philos. Soc. 123:4222–34 [Google Scholar]
  66. Wiens JJ. 2001. Widespread loss of sexually selected traits: how the peacock lost its spots. Trends Ecol. Evol. 16:9517–23 [Google Scholar]
  67. Wilkinson GS, Johns PM, Metheny JD, Baker RH. 2013. Sex-biased gene expression during head development in a sexually dimorphic stalk-eyed fly. PLOS ONE 8:3e59826 [Google Scholar]
  68. Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB. 2008. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134:4610–23 [Google Scholar]
  69. Wright D, Boije H, Meadows JRS, Bed'hom B, Gourichon D. et al. 2009. Copy number variation in intron 1 of SOX5 causes the pea-comb phenotype in chickens. PLOS Genet. 5:6e1000512 [Google Scholar]
  70. Zuk M, Johnsen TS, Maclarty T. 1995. Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc. R. Soc. Lond. B-Biol. Sci. 260:1358205–10 [Google Scholar]
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