Skip to main content

Cryptic Female Choice and Other Types of Post-copulatory Sexual Selection

  • Chapter
  • First Online:
Cryptic Female Choice in Arthropods

Abstract

This chapter discusses sexual selection by cryptic female choice (CFC) and other possible types of selection on traits involved in male–female interactions during and following copulation. Morphological, behavioral, and probably also physiological traits all show the typical earmarks of sexual selection: puzzlingly extravagant, apparently non-utilitarian design; and rapid divergent evolution. I discuss ways to attempt to distinguish CFC from other possibilities, and their potential overlap. Differentiating narrow-sense from broad-sense male–female conflict may help clear up some current confusion. The most central differences between the leading hypotheses concern the expected effects of selectively granting paternity on a female’s fitness. Unfortunately, convincing tests of these effects have not been feasible due to technical limitations; published claims regarding such measurements must be treated with caution. Several types of data that provide less direct tests, including defensive designs of females, the presence of female sense organs specialized to sense courtship stimuli from males, physical damage inflicted on the female by the male during copulation, and physical male–female struggles, are discussed. Different types of selection may operate simultaneously in some species, and all may be applicable in particular cases; the major questions concern the relative frequencies of species in which each type of selection occurs. The hypotheses nevertheless provide useful theoretical contexts for understanding multiple aspects of reproductive biology. One promising area for future studies, in which arthropods can provide both experimental and comparative data, is the role of non-genitalic male copulatory courtship structures in stimulating or physically coercing females during sexual interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aisenberg A, Barrantes G, Eberhard WG (2015) Post-copulatory sexual selection in two tropical orb-weaving leucauge spiders. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Alexander RD, Marshall DC, Cooley JR (1997) Evolutionary perspectives on insect mating. In: Choe JC, Crespie BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 4–31

    Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Andrés JA, Cordero-Rivera A (2000) Copulation duration and fertilization success in a damselfly: an example of cryptic female choice? Anim Behav 59:695–703

    Article  PubMed  Google Scholar 

  • Arnqvist G (2014) Cryptic female choice. In: Shuker D, Simmons LW (eds) The evolution of insect mating systems. Oxford University Press, New York, pp 204–220

    Chapter  Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton

    Book  Google Scholar 

  • Baena M, Eberhard WG (2007) Appearances deceive: female “resistance” behaviour in a sepsid fly is not a test of male ability to hold on. Ethol Ecol Evol 19:27–50

    Article  Google Scholar 

  • Barbosa F (2015) An integrative view of postcopulatory sexual selection in a soldier fly: interplay between cryptic mate choice and sperm competition. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Baker RR, Bellis MA (1995) Human sperm competition, copulation masturbation and infidelity. Chapman and Hall, New York

    Google Scholar 

  • Birkhead TR (1998) Cryptic female choice: criteria for establishing female sperm choice. Evolution 52:212–1218

    Article  Google Scholar 

  • Birkhead TR, Møller AP (1992) Sperm competition in birds—evolutionary causes and consequences. Academic Press, New York

    Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, NY

    Google Scholar 

  • Brennan PLR, Prum RO (2012) The limits of sexual conflict in the narrow sense: new insights from waterfowl biology. Phil. Trans. R. Soc. B 367:2324–2338

    Article  PubMed Central  PubMed  Google Scholar 

  • Briceño RD, Eberhard WG (2015) Species-specific behavioral differences in male tsetse fly genital morphology and probable cryptic female choice. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Calbacho-Rosa L, Peretti AV (2015) Copulatory and post-copulatory sexual selection in haplogyne spiders, with emphasis on Pholcidae and Oonopidae. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Christy J (1995) Mimicry mate choice and the sensory trap hypothesis. Am Nat 146:171–181

    Google Scholar 

  • Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22

    Article  CAS  PubMed  Google Scholar 

  • Cordero C, Eberhard WG (2005) Interaction between sexually antagonistic selection and mate choice in the evolution of female responses to male traits. Evol Ecol 19:111–122

    Article  Google Scholar 

  • Cordero-Rivera A, Córdoba-Aguilar A (2010) Selective forces propelling genitalia evolution in Odonata. In: Leonard J, Córdoba-Aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University Press, New York, pp 332–352

    Google Scholar 

  • Córdoba-Aguilar A (2003) Predicting mechanisms of sperm displacement based on genital morphometrics in the Calopterygidae (Odonata). J Ins Behav 16:153–167

    Google Scholar 

  • Córdoba-Aguilar A (2005) Possible coevolution of male and female genital form and function in a calopterygid damselfly. J Evol Biol 18:132–137

    Article  PubMed  Google Scholar 

  • Córdoba-Aguilar A, González-Tokman D, Nava-Bolaños A, Cuevas-Yáñez K, Rivas M (2015) Female choice in damselflies and dragonflies. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Crudgington H, Siva-Jothy M (2000) Genital damage, kicking and early death. Nature 407:855–856

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1871) The descent of man and selection in relation to sex, 6th edn. Reprinted. Modern Library, New York

    Google Scholar 

  • Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Eberhard WG (1992) Courtship before and during copulation by three species of Macrodactylus (Coleoptera, Scarabeidae, Melolonthinae). Ethol Ecol Evol 5:19–63

    Article  Google Scholar 

  • Eberhard WG (1994) Evidence for widespread courtship during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution 48:711–733

    Article  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Eberhard WG (2001) The functional morphology of species-specific clasping structures on the front legs of male Archisepsis and Palaeosepsis flies (Diptera, Sepsidae). Zool J Linn Soc 133:335–368

    Article  Google Scholar 

  • Eberhard WG (2002) The function of female resistance behavior: intromission by male coercion vs. female cooperation in sepsid flies (Diptera: Sepsidae). Rev Biol Trop 50:485–505

    PubMed  Google Scholar 

  • Eberhard WG (2004a) Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice. Evolution 58:1947–1970

    Article  PubMed  Google Scholar 

  • Eberhard WG (2004b) Male–female conflict and genitalia: failure to confirm predictions in insects and spiders. Biol Rev 79:121–186

    Article  PubMed  Google Scholar 

  • Eberhard WG (2009) Postcopulatory sexual selection: Darwin’s omission and its consequences. Proc Nat Acad Sci USA 106(Suppl 1):10025–10032

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eberhard WG (2010) Evolution of genitalia: theories, evidence, and new directions. Genetica 138:5–18

    Article  PubMed  Google Scholar 

  • Eberhard WG (2012) Experiments with genitalia: a commentary. Trends Ecol Evol 26:7–21

    Google Scholar 

  • Eberhard WG, Ramirez N (2004) Functional morphology of the male genitalia of four species of Drosophila: failure to confirm both lock and key and male-female conflict predictions. Ann Ent Soc Am 97:1007–1017

    Article  Google Scholar 

  • Eberhard WG, Huber BA, Rodriguez RL, Briceño RD, Solis I, Rodriguez V (1998) One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution 52:415–431

    Article  Google Scholar 

  • Emlen M, Warren IA, Johns A, Dworkin I, Lavine LC (2012) A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337:860–864

    Article  CAS  PubMed  Google Scholar 

  • Flowers W, Eberhard WG (2006) Fitting together: copulatory linking in some Neotropical Chrysomeloidae. Rev Biol Trop 54:829–842

    Google Scholar 

  • Holland B, Rice W (1998) Chase-away sexual selection: antagonistic seduction vs resistance. Evolution 52:1–7

    Article  Google Scholar 

  • Hotzy C, Polak M, Rönn JL, Arnqvist G (2012) Phenotype engineering unveils the function of genital morphology. Curr Biol 22:2258–2261

    Article  CAS  PubMed  Google Scholar 

  • Jennions MD (2005) Sexual tension: does conflict lead to costly mate choice? Evolution 60:415–417

    Google Scholar 

  • Kamimura Y (2007) Twin intromittent organs of Drosophila for traumatic insemination. Biol Lett 3:401–404

    Article  PubMed Central  PubMed  Google Scholar 

  • Kamimura Y (2010) Copulation anatomy of Drosophila melanogaster (Diptera: Drosophilidae): wound-making organs and their possible roles. Zoomorphology 1129:163–174

    Article  Google Scholar 

  • Kamimura Y (2015) What is indirect cryptic female choice? Theoretical considerations and an example from a promiscuous earwig. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Kamimura Y, Mitsumoto H (2012) Lock-and-key structural isolation between sibling Drosophila species. Ent Sci 15:197–201

    Article  Google Scholar 

  • Kamimura Y, Polak M (2010) Does surgical manipulation of Drosophila intromittent organs affect insemination success? Proc R Soc B Biol Sci 278:815–816

    Article  Google Scholar 

  • Karn RC, Clark NL, Nguyen ED, Swanson WJ (2008) Adaptive evolution in rodent seminal vesicle secretion proteins. Molec Biol Evol 25:2301–2310

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kokko H, Jennions MD (2014) The relationship between sexual selection and sexual conflict. In: Rice W, Gavrilets S (eds) Additional perspectives on the genetics and biology of sexual conflict. Cold Spring Harb Perspect Biol, Woodbury 6(9):a017517

    Google Scholar 

  • Kokko H, Brooks R, Jennions MD, Morly J (2003) The evolution of mate choice and mating biases. Proc R Soc B Biol Sci 270:653–664

    Article  Google Scholar 

  • Krieger F, Krieger-Loibl E (1958) Beitrage zum Verhalten von Ischnura elegans und Ischnura pumilio (Odonata). Z Tierpsychol 15:82–93

    Article  Google Scholar 

  • Lachaise D, Harry M, Solignac M, Lemeunier F, Bénassi, V Cariou ML (2000) Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomó. Proc R Soc B Biol Sci 267:1487–1495

    Google Scholar 

  • Lange R, Reinhardt K, Michaels NK, Anthes N (2013) Functions, diversity, and evolution of traumatic mating. Biol Rev 88:585–601

    Article  PubMed  Google Scholar 

  • Leonard J, Córdoba-Aguilar A (2010) The evolution of primary sexual characters in animals. Oxford University Press, New York

    Google Scholar 

  • Masly JP, Kamimura Y (2014) Asymmetric mismatch in strain-specific genital morphology causes increased harm to Drosophila females. Evolution. doi:10.1111/evo.12436

    PubMed  Google Scholar 

  • Massoiud Z, Betsch J-M (1972) Étude sur les insectes collemboles, II: les caractéres sexuels secondaires des antennes des Symphypléones. Rev. Ecol. Biol. Sol 9:55–97

    Article  Google Scholar 

  • Mayer H (1957) Zur Biologie und Ethologie einheimischer Collembolen. Zool. Jahrb. Abt. System. 85:501–570

    Google Scholar 

  • McPeek M, Shen AL, Torrey JZ, Farid H (2008) The tempo and mode of 3-dimensional morphological evolution in male reproductive structures. Am Nat 171:E158–E178

    Article  PubMed  Google Scholar 

  • McPeek MA, Shen L, Farid H (2009) The correlated evolution of three-dimensional reproductive structures between male and female damselflies. Evolution 63:73–83

    Article  PubMed  Google Scholar 

  • Miller PL (1984) The structure of the genitalia and th volumes of sperm stored in male and female Nesciothemis farinosa (Foerster) and Orthetrum chrysostigma (Burmeister) (Anisoptera: Libellulidae). Odonatologica 13:415–428

    Google Scholar 

  • Miller PL (1990) Mechanisms of sperm removal and sperm transfer in Orthetrum coerulescens (Fabricius) (Odonata: Libellulidae). Physiol Ent 15:199–209

    Article  Google Scholar 

  • Møller AP (1997) Female control; sexual selection by cryptic female choice. uart Rev Biol 72:202–203 By William G. Eberhard

    Article  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Peretti AV (2010) An ancient indirect sex model. Single and mixed patterns in the evolution of scorpion genitalia. In: Leonard J, Córdoba-Aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University Press. New York, pp 218–248

    Google Scholar 

  • Peretti A, Córdoba-Aguilar A (2007) On the value of fine-scaled behavioural observations for studies of sexual coercion. Ethol Ecol Evol 19:77–86

    Article  Google Scholar 

  • Polak M, Rashad A (2010) Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proc R Soc B Biol Sci 277:1371–1376

    Article  Google Scholar 

  • Robertson RR, Paterson HEH (1982) Mate recognition and mechanical isolation in Enallagma damselflies. Evolution 36:243–250

    Article  Google Scholar 

  • Schneider J, Uhl G, Herberstein ME Cryptic female choice within the genus Argiope: a comparative approach. Chapter 3 this volume

    Google Scholar 

  • Shapiro AM, Porter AH (1989) The lock and key hypothesis: evolutionary and biosystematics interpretations of insect genitalia. Ann Rev Ent 34:231–245

    Article  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Simmons LW (2014) Sexual selection and genital evolution. Austral Entom 53:1–17

    Article  Google Scholar 

  • Sirot L, Wolfner M (2015) Who’s zooming who? Seminal fluids and cryptic female choice in diptera. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods. Springer, Cham

    Google Scholar 

  • Smith R (1984) Sperm competition and the evolution of animal mating systems. Academic Press, New York

    Google Scholar 

  • Sota T, Kubota K (1998) Genital lock-and-key as a selective agent against hybridization. Evolution 52:507–1513

    Article  Google Scholar 

  • Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144

    Article  CAS  PubMed  Google Scholar 

  • Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquando CF (2001) Evolutionary EST analysis identifies rapidly evolving male reproductive products in Drosophila. Proc Nat Acad Sci USA 98:7375–7379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20:18–20

    Google Scholar 

  • Tallamy DW, Powell BE, McClafferty (2002) Male traits under cryptic female choice in the spotted cucumber beetle (Coleoptera: Chrysomelidae). Behav Ecol 13:511–518

    Google Scholar 

  • Tallamy DW, Darlington MB, Pesek JD, Powell BE (2003) Copulatory courtship signals male genetic quality in cucumber beetles. Proc R Soc B Biol Sci 270:77–82

    Article  Google Scholar 

  • Thornhill R (1983) Cryptic female choice and its implications for the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788

    Article  Google Scholar 

  • West-Eberhard MJ (2014) Darwin’s forgotten idea: the social essence of sexual selection. Neurosci Biobehav Rev 46:501–508

    Article  PubMed  Google Scholar 

  • Wiley RH, Poston J (1996) Indirect mate choice: competition for mates and coevolution of the sexes. Evolution 50:1371–1381

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, Princeton

    Google Scholar 

  • Williams GC (1997) The pony fish’s glow: and other clues to plan and purpose in nature. Basic Books, New York

    Google Scholar 

  • Yassin A, Orgogozo V (2013) Coevolution between male and female genitalia in the Drosophila melanogaster species subgroup. PLoS ONE 8(2):e57158

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zigler KS (2008) The evolution of sea urchin sperm binding. Int J Develop Biol 52:791–796

    Article  CAS  Google Scholar 

  • Zigler KS, Lesios HA (2003) Evolution of binding in the pantropical sea urchin Tripneustes: comparisons to binding of other genera. Mol Biol Evol 20:220–231

    Article  CAS  PubMed  Google Scholar 

  • Zimmer C, Emlen D (2013) Evolution: making sense of life. Roberts, Greenwood Village

    Google Scholar 

  • Zinkl GM, Zwiebel BI, Grier DG, Preuss D (1999) Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development 126:5431–5440

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I thank Anita Aisenberg and Alfredo Peretti for the invitation to write this chapter; Y. Kamimura, M.J. West-Eberhard, M. Jennions, R.L. Rodriguez, and A. Aisenberg for useful comments on a preliminary draft; and the Smithsonian Tropical Research Institute and the Universidad de Costa Rica for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to William G. Eberhard .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Eberhard, W.G. (2015). Cryptic Female Choice and Other Types of Post-copulatory Sexual Selection. In: Peretti, A., Aisenberg, A. (eds) Cryptic Female Choice in Arthropods. Springer, Cham. https://doi.org/10.1007/978-3-319-17894-3_1

Download citation

Publish with us

Policies and ethics