Evolutionary Ecology

, 23:93 | Cite as

Female polymorphisms, sexual conflict and limits to speciation processes in animals

  • Erik I. Svensson
  • Jessica K. Abbott
  • Thomas P. Gosden
  • Audrey Coreau
Original Paper


Heritable and visually detectable polymorphisms, such as trophic polymorphisms, ecotypes, or colour morphs, have become classical model systems among ecological geneticists and evolutionary biologists. The relatively simple genetic basis of many polymorphisms (one or a few loci) makes such species well-suited to study evolutionary processes in natural settings. More recently, polymorphic systems have become popular when studying the early stages of the speciation process and mechanisms facilitating or constraining the evolution of reproductive isolation. Although colour polymorphisms have been studied extensively in the past, we argue that they have been underutilized as model systems of constraints on speciation processes. Colouration traits may function as signalling characters in sexual selection contexts, and the maintenance of colour polymorphisms is often due to frequency-dependent selection. One important issue is why there are so few described cases of female polymorphisms. Here we present a synthetic overview of female sexual polymorphisms, drawing from our previous work on female colour polymorphisms in lizards and damselflies. We argue that female sexual polymorphisms have probably been overlooked in the past, since workers have mainly focused on male-male competition over mates and have not realized the ecological sources of genetic variation in female fitness. Recent experimental evolution studies on fruit flies (Drosophila melanogaster) have demonstrated significant heritable variation among female genotypes in the fitness costs of resistance or tolerance to male mating harassment. In addition, female-female competition over resources could also generate genetic variation in female fitness and promote the maintenance of female sexual polymorphisms. Female sexual polymorphisms could subsequently either be maintained as intrapopulational polymorphisms or provide the raw material for the formation of new species.


Antagonistic coevolution Female competition Female resistance Male mating harassment Sexual conflict Speciation 



This study was financially supported by grants from the Swedish Research Council (VR), and The Swedish Council for Environment, Agriculture and Spatial Planning (FORMAS) to E. I. S. We are grateful to Fabrice Eroukhmanoff, Roger Härdling, Kristina Karlsson, Anna Runemark and other members of our research laboratory for stimulating discussions on female polymorphisms over the past years, and to three anonymous referees for criticisms on the first version of this manuscript. We also wish to thank Ola Fincke for providing us with a pre-print of her recent paper that was in press when we finished this article.


  1. Abbott J, Svensson EI (2005) Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly. J Evol Biol 18:1464–1470PubMedGoogle Scholar
  2. Abbott JK, Svensson EI (2007) Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs. Evol Ecol doi: 10.1007/s10682-007-9161-0 Google Scholar
  3. Ågren J, Ericson L (1996) Population structure and morph-specific fitness differences in tristylous Lythrum salicaria. Evolution 50:126–139Google Scholar
  4. Andrés JA, Sánchez-Guillen RA, Cordero Rivera A (2000) Molecular evidence for selection on female color polymorphism in the damselfly Ischnura graellsii. Evolution 54:2156–2161PubMedGoogle Scholar
  5. Arnqvist G, Edwardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. Proc Natl Acad Sci USA 97:10460–10464PubMedGoogle Scholar
  6. Arnqvist G, Rowe L (2002) Antagonistic coevolution between the sexes in a group of insects. Nature 415:787–789PubMedGoogle Scholar
  7. Barrett SCH (1998) The reproductive biology and genetics of island plants. In: Grant PR (ed) Evolution on islands. Oxford University Press, Oxford, pp 18–34Google Scholar
  8. Bateman AJ (1948) Intra-Sexual selection in Drosophila. Heredity 2:349–368PubMedGoogle Scholar
  9. Bleiweiss R (2001) Asymmetrical expression of transsexual phenotypes in hummingbirds. Proc R Soc Lond B 268:639–646Google Scholar
  10. Bond AB, Kamil AC (1998) Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature 395:594–596Google Scholar
  11. Bond AB, Kamil AC (2002) Visual predators select for crypticity and polymorphism in virtual prey. Nature 415:609–613PubMedGoogle Scholar
  12. Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339PubMedGoogle Scholar
  13. Brommer JE, Ahola K, Karstinen T (2005) The colour of fitness: plumage coloration and lifetime reproductive success in the tawny owl. Proc R Soc B-Biol Sci 272:935–940Google Scholar
  14. Byrne PG, Rice WR (2006) Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc R Soc B-Biol Sci 273:917–922Google Scholar
  15. Cordero A (1990) The inheritance of female polymorphism in the damselfly Ischnura graellsii (Rambur)(Odonata:Coenagrionidae). Heredity 64:341–346Google Scholar
  16. Cordero A, Carbone SS, Utzeri C (1998) Mating opportunities and mating costs are reduced in androchrome female damselflies, Ischnura elegans. Anim Behav 55:185–187PubMedGoogle Scholar
  17. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates Inc., Sunderland, MassachusettsGoogle Scholar
  18. Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357PubMedGoogle Scholar
  19. Dieckmann U, Doebeli M (2005) Pluralism in evolutionary theory. J Evol Biol 18:1209–1213PubMedGoogle Scholar
  20. Dobzhansky T (1970) Genetics of the evolutionary process. Columbia University Press, New yorkGoogle Scholar
  21. Doebeli M, Dieckmann U (2000) Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am Nat 156:S45–S61Google Scholar
  22. Eckert CG, Barrett CH (1995) Style morph ratios in tristylous Decodon verticillatus (Lythraceae): selection vs. historical contingency. Ecology 76:1051–1066Google Scholar
  23. Ellers J, Boggs CL (2003) The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies. Evolution 57:1100–1106PubMedGoogle Scholar
  24. Felsenstein J (1981) Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124–138Google Scholar
  25. Fincke OM (2004) Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Anim Behav 67:833–845Google Scholar
  26. Fincke OM, Jödicke R, Paulson D, Schultz DT (2005) The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like morphs typically the minority? Int J Odonatol 8:183–212Google Scholar
  27. Fincke OM, Fargevieille A, Schultz TD (2007) Lack of innate preference for morph and species identity in mate-searching Enallagma damselflies. Behav Ecol Sociobiol 61:1121–1131Google Scholar
  28. Ford EB (1975) Ecological genetics 4th edn. Chapman and Hall, LondonGoogle Scholar
  29. Gavrilets S (2000) Rapid evolution of reproductive barriers by sexual conflict. Nature 403:886–889PubMedGoogle Scholar
  30. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton University Press, NJ, PrincetonGoogle Scholar
  31. Gavrilets S, Waxman D (2002) Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA 99:10533–10538PubMedGoogle Scholar
  32. Gosden TP, Svensson EI (2007) Female sexual polymorphism and fecundity consequences of male mating harassment in the wild. PLoS ONE 2(6):e580 doi:10.1371/journal.pone.0000580Google Scholar
  33. Gray SM, McKinnon JS (2007) Linking color polymorphism maintenance and speciation. Trends Ecol Evol 22:71–79PubMedGoogle Scholar
  34. Gross MR (1985) Disruptive selection for alternative life histories in Salmon. Nature 313:47–48Google Scholar
  35. Hardling R, Bergsten J (2006) Nonrandom mating preserves intrasexual polymorphism and stops population differentiation in sexual conflict. Am Nat 167:401–409PubMedGoogle Scholar
  36. Hayashi TI, Vose M, Gavrilets S (2007) Genetic differentiation by sexual conflict. Evolution 61:516–529PubMedGoogle Scholar
  37. Higashi M, Takimoto G, Yanamura N (1999) Sympatric speciation by sexual selection. Nature 402:523–526PubMedGoogle Scholar
  38. Higgie M, Chenoweth S, Blows MW (2000) Natural selection and the reinforcement of mate recognition. Science 290:519–521PubMedGoogle Scholar
  39. Houle D (1991) Genetic covariance of fitness correlates: what genetic correlations are matters. Evolution 45:630–648Google Scholar
  40. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204PubMedGoogle Scholar
  41. Houle D, Hughes KA, Hoffmaster DK, Ihara J, Assimacopoulus S, Canada D, Charlesworth B (1994) The effects of spontaneous mutation on quantitative traits. I. Variances and covariances of life history traits. Genetics 138:773–785PubMedGoogle Scholar
  42. Johnson C (1975) Polymorphism and natural selection in Ischnuran damselflies. Evol Theory 1:81–90Google Scholar
  43. Joron M, Brakefield PM (2003) Captivity masks inbreeding effects on male mating success in butterflies. Nature 424:191–194PubMedGoogle Scholar
  44. Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261PubMedGoogle Scholar
  45. Kirkpatrick M (1982) Sexual selection and the evolution of female choice. Evolution 36:1–12Google Scholar
  46. Kokko H (2001) Fisherian and “good genes” benefits of mate choice: how (not) to distinguish between them. Ecol Lett 4:322–326Google Scholar
  47. Kokko H (2005) Useful ways of being wrong. J Evol Biol 18:1155–1157PubMedGoogle Scholar
  48. Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection continuum. Proc R Soc Lond B 269:1331–1340Google Scholar
  49. Kopp M, Hermisson J (2006) The evolution of genetic architecture under frequency-dependent disruptive selection. Evolution 60:1537–1550PubMedGoogle Scholar
  50. Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334Google Scholar
  51. Lande R, Seehausen O, van Alphen JM (2001) Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112–113:435–443PubMedGoogle Scholar
  52. Lank DB, Smith CM, Hanotte O, Burke T, Cooke F (1995) Genetic polymorphism for alternative mating-behavior in Lekking male Ruff Philomachus-Pugnax. Nature 378:59–62Google Scholar
  53. Leimar O (2005) The evolution of phenotypic polymorphism: randomized strategies versus evolutionary branching. Am Nat 165:669–681PubMedGoogle Scholar
  54. Lew TA, Morrow EH, Rice WR (2006) Standing genetic variance for female resistance to harm from males and its relationship to intralocus sexual conflict. Evolution 60:97–105PubMedGoogle Scholar
  55. Linder JE, Rice WR (2005) Natural selection and genetic variation for female resistance to harm from males. J Evol Biol 18:568–575PubMedGoogle Scholar
  56. Magurran AE (1998) Population differentiation without speciation. Phil Trans R Soc Lond B 353:275–286Google Scholar
  57. Maynard Smith J (1982) Evolution and the theory of games. Cambridge University Press, CambridgeGoogle Scholar
  58. Maynard Smith J (1996) The games lizards play. Nature 380:198–199Google Scholar
  59. McKinnon JS, Demayo RF, Granquist R, Weggel L (2000) Female red throat coloration in two populations of threespine stickleback. Behaviour 137:947–963Google Scholar
  60. Nielsen MG, Watt WB (2000) Interference competition and sexual selection promote polymorphism in Colias (Lepidoptera, Pieridae). Funct Ecol 14:718–730Google Scholar
  61. Noor MA (1995) Speciation driven by natural selection in Drosophila. Nature 375:674–675PubMedGoogle Scholar
  62. Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci USA 98:12084–12088PubMedGoogle Scholar
  63. Nosil P, Crespi BJ (2004) Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks. Evolution 58:102–112PubMedGoogle Scholar
  64. Nosil P, Crespi BJ, Sandoval CP (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:440–443PubMedGoogle Scholar
  65. Palumbi SR (1999) All males are not created equal: fertility differences depend on game recognition polymorphisms in sea urchins. Proc Natl Acad Sci USA 96:12632–12637PubMedGoogle Scholar
  66. Parker GA, Partridge L (1998) Sexual conflict and speciation. Phil Trans R Soc Lond B 353:261–274Google Scholar
  67. Pierotti MER, Seehausen O (2007) Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids. J Evol Biol 20:240–248PubMedGoogle Scholar
  68. Rhen T (2000) Sex-limited mutations and the evolution of sexual dimorphism. Evolution 54:37–43PubMedGoogle Scholar
  69. Rice WR (1994) Degeneration of a nonrecombining chromosome. Science 263:230–232PubMedGoogle Scholar
  70. Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–234PubMedGoogle Scholar
  71. Rice WR (1998) Intergenomic conflict, interlocus antagonistic coevolution and the evolution of reproductive isolation. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, OxfordGoogle Scholar
  72. Rice WR, Holland B (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav Ecol Sociobiol 41:1–10Google Scholar
  73. Rice WR, Chippindale AK (2001) Intersexual ontogenetic conflict. J Evol Biol 14:685–693Google Scholar
  74. Rice AM, Pfennig DW (2007) Character displacement: in situ evolution of novel phenotypes or sorting of pre-existing variation? J Evol Biol 20:448–459PubMedGoogle Scholar
  75. Robinson BW, Schluter D (2000) Natural selection and the evolution of adaptive genetic variation in northern freshwater fishes. In: Mousseau TA, Sinervo B, Endler JA (eds) Adaptive genetic variation in the wild. Oxford University Press, Oxford, pp 65–94Google Scholar
  76. Roulin A, Ducret B, Ravussin PA, Altwegg R (2003) Female colour polymorphism covaries with reproductive strategies in the tawny owl Strix aluco. J Avian Biol 34:393–401Google Scholar
  77. Rowe L, Arnqvist G (2002) Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to adress evolutionary processes. Evolution 56:754–767PubMedGoogle Scholar
  78. Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263:1415–1421Google Scholar
  79. Rueffler C, Van Dooren TJM, Leimar O, Abrams PA (2006) Disruptive selection and then what? Trends Ecol Evol 21:238–245PubMedGoogle Scholar
  80. Sanchez-Guillen RA, Van Gossum H, Rivera AC (2005) Hybridization and the inheritance of female colour polymorphism in two ischnurid damselflies (Odonata:Coenagrionidae). Biol J Linn Soc 85:471–481Google Scholar
  81. Schemske DW, Bierzychudek P (2001) Perspective: evolution of flower color in the desert annual Linanthus parryae: Wright revisited. Evolution 55:1269–1282PubMedGoogle Scholar
  82. Schluter D (1998a) Ecological causes of speciation. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 114–129Google Scholar
  83. Schluter D (1998b) Ecological speciation in postglacial fishes. In: Grant PR (ed) Evolution on islands. Oxford University Press, Oxford, pp 163–180Google Scholar
  84. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  85. Schluter D, Price T, Mooers AO, Ludwig D (1997) Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–1711Google Scholar
  86. Shuster SM, Sassaman C (1997) Genetic interaction between male mating strategy and sex ratio in a marine isopod. Nature 388:373–377Google Scholar
  87. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, PrincetonGoogle Scholar
  88. Sinervo B, Lively CM (1996) The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380:240–243Google Scholar
  89. Sinervo B, Svensson E, Comendant T (2000) Density cycles and an offspring quantity and quality game driven by natural selection. Nature 406:985–988PubMedGoogle Scholar
  90. Smith TB (1993) Disruptive selection and the genetic basis of bill size polymorphism in the African finch Pyrenestes. Nature 363:618–6120Google Scholar
  91. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedGoogle Scholar
  92. Svensson E, Sinervo B, Comendant T (2001) Density-dependent competition and selection on immune function in genetic lizard morphs. Proc Natl Acad Sci USA 98:12561–12565PubMedGoogle Scholar
  93. Svensson EI, Abbott J (2005) Evolutionary dynamics and population biology of a polymorphic insect. J Evol Biol 18:1503–1514PubMedCrossRefGoogle Scholar
  94. Svensson EI, Abbott J, Hardling R (2005) Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations. Am Nat 165:567–576PubMedGoogle Scholar
  95. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 137–179Google Scholar
  96. Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343PubMedGoogle Scholar
  97. Van Dooren TJM (1999) The evolutionary ecology of dominance-recessivity. J Theor Biol 198:519–532PubMedGoogle Scholar
  98. Van Gossum H, Stoks R, De Bruyn L (2001) Reversible frequency-dependent switches in male mate choice. Proc R Soc Lond B 268:83–85Google Scholar
  99. Vercken E, Massot M Sinervo B, Clobert J (2007) Colour variation and alternative reproductive strategies in females of the common lizard Lacerta vivipara. J Evol Biol 20:221–232PubMedGoogle Scholar
  100. Waxman D, Gavrilets S (2005a) 20 questions on adaptive dynamics. J Evol Biol 18:1139–1154PubMedGoogle Scholar
  101. Waxman D, Gavrilets S (2005b) Issues of terminology, gradient dynamics and the ease of sympatric speciation in Adaptive Dynamics. J Evol Biol 18:1214–1219PubMedGoogle Scholar
  102. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  103. Wright S (1969) Evolution and the genetics of populations. Volume 2. The theory of gene frequencies. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Erik I. Svensson
    • 1
  • Jessica K. Abbott
    • 2
  • Thomas P. Gosden
    • 1
  • Audrey Coreau
    • 3
  1. 1.Section for Animal Ecology, Ecology BuildingLund UniversityLundSweden
  2. 2.Department of BiologyQueen’s UniversityKingstonCanada
  3. 3.Centre d’Ecologie Fonctionnelle et Evolutive (CEFE-CNRS, UMR 5175)Montpellier Cedex 5France

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