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.
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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
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
Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ
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
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
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
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
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
Baker RR, Bellis MA (1995) Human sperm competition, copulation masturbation and infidelity. Chapman and Hall, New York
Birkhead TR (1998) Cryptic female choice: criteria for establishing female sperm choice. Evolution 52:212–1218
Birkhead TR, Møller AP (1992) Sperm competition in birds—evolutionary causes and consequences. Academic Press, New York
Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, NY
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
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
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
Christy J (1995) Mimicry mate choice and the sensory trap hypothesis. Am Nat 146:171–181
Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22
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
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
Córdoba-Aguilar A (2003) Predicting mechanisms of sperm displacement based on genital morphometrics in the Calopterygidae (Odonata). J Ins Behav 16:153–167
Córdoba-Aguilar A (2005) Possible coevolution of male and female genital form and function in a calopterygid damselfly. J Evol Biol 18:132–137
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
Crudgington H, Siva-Jothy M (2000) Genital damage, kicking and early death. Nature 407:855–856
Darwin C (1871) The descent of man and selection in relation to sex, 6th edn. Reprinted. Modern Library, New York
Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge
Eberhard WG (1992) Courtship before and during copulation by three species of Macrodactylus (Coleoptera, Scarabeidae, Melolonthinae). Ethol Ecol Evol 5:19–63
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
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
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
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
Eberhard WG (2004a) Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice. Evolution 58:1947–1970
Eberhard WG (2004b) Male–female conflict and genitalia: failure to confirm predictions in insects and spiders. Biol Rev 79:121–186
Eberhard WG (2009) Postcopulatory sexual selection: Darwin’s omission and its consequences. Proc Nat Acad Sci USA 106(Suppl 1):10025–10032
Eberhard WG (2010) Evolution of genitalia: theories, evidence, and new directions. Genetica 138:5–18
Eberhard WG (2012) Experiments with genitalia: a commentary. Trends Ecol Evol 26:7–21
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
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
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
Flowers W, Eberhard WG (2006) Fitting together: copulatory linking in some Neotropical Chrysomeloidae. Rev Biol Trop 54:829–842
Holland B, Rice W (1998) Chase-away sexual selection: antagonistic seduction vs resistance. Evolution 52:1–7
Hotzy C, Polak M, Rönn JL, Arnqvist G (2012) Phenotype engineering unveils the function of genital morphology. Curr Biol 22:2258–2261
Jennions MD (2005) Sexual tension: does conflict lead to costly mate choice? Evolution 60:415–417
Kamimura Y (2007) Twin intromittent organs of Drosophila for traumatic insemination. Biol Lett 3:401–404
Kamimura Y (2010) Copulation anatomy of Drosophila melanogaster (Diptera: Drosophilidae): wound-making organs and their possible roles. Zoomorphology 1129:163–174
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
Kamimura Y, Mitsumoto H (2012) Lock-and-key structural isolation between sibling Drosophila species. Ent Sci 15:197–201
Kamimura Y, Polak M (2010) Does surgical manipulation of Drosophila intromittent organs affect insemination success? Proc R Soc B Biol Sci 278:815–816
Karn RC, Clark NL, Nguyen ED, Swanson WJ (2008) Adaptive evolution in rodent seminal vesicle secretion proteins. Molec Biol Evol 25:2301–2310
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
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
Krieger F, Krieger-Loibl E (1958) Beitrage zum Verhalten von Ischnura elegans und Ischnura pumilio (Odonata). Z Tierpsychol 15:82–93
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
Lange R, Reinhardt K, Michaels NK, Anthes N (2013) Functions, diversity, and evolution of traumatic mating. Biol Rev 88:585–601
Leonard J, Córdoba-Aguilar A (2010) The evolution of primary sexual characters in animals. Oxford University Press, New York
Masly JP, Kamimura Y (2014) Asymmetric mismatch in strain-specific genital morphology causes increased harm to Drosophila females. Evolution. doi:10.1111/evo.12436
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
Mayer H (1957) Zur Biologie und Ethologie einheimischer Collembolen. Zool. Jahrb. Abt. System. 85:501–570
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
McPeek MA, Shen L, Farid H (2009) The correlated evolution of three-dimensional reproductive structures between male and female damselflies. Evolution 63:73–83
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
Miller PL (1990) Mechanisms of sperm removal and sperm transfer in Orthetrum coerulescens (Fabricius) (Odonata: Libellulidae). Physiol Ent 15:199–209
Møller AP (1997) Female control; sexual selection by cryptic female choice. uart Rev Biol 72:202–203 By William G. Eberhard
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567
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
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
Polak M, Rashad A (2010) Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proc R Soc B Biol Sci 277:1371–1376
Robertson RR, Paterson HEH (1982) Mate recognition and mechanical isolation in Enallagma damselflies. Evolution 36:243–250
Schneider J, Uhl G, Herberstein ME Cryptic female choice within the genus Argiope: a comparative approach. Chapter 3 this volume
Shapiro AM, Porter AH (1989) The lock and key hypothesis: evolutionary and biosystematics interpretations of insect genitalia. Ann Rev Ent 34:231–245
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, NJ
Simmons LW (2014) Sexual selection and genital evolution. Austral Entom 53:1–17
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
Smith R (1984) Sperm competition and the evolution of animal mating systems. Academic Press, New York
Sota T, Kubota K (1998) Genital lock-and-key as a selective agent against hybridization. Evolution 52:507–1513
Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144
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
Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20:18–20
Tallamy DW, Powell BE, McClafferty (2002) Male traits under cryptic female choice in the spotted cucumber beetle (Coleoptera: Chrysomelidae). Behav Ecol 13:511–518
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
Thornhill R (1983) Cryptic female choice and its implications for the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788
West-Eberhard MJ (2014) Darwin’s forgotten idea: the social essence of sexual selection. Neurosci Biobehav Rev 46:501–508
Wiley RH, Poston J (1996) Indirect mate choice: competition for mates and coevolution of the sexes. Evolution 50:1371–1381
Williams GC (1966) Adaptation and natural selection: a critique of some current evolutionary thought. Princeton University Press, Princeton
Williams GC (1997) The pony fish’s glow: and other clues to plan and purpose in nature. Basic Books, New York
Yassin A, Orgogozo V (2013) Coevolution between male and female genitalia in the Drosophila melanogaster species subgroup. PLoS ONE 8(2):e57158
Zigler KS (2008) The evolution of sea urchin sperm binding. Int J Develop Biol 52:791–796
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
Zimmer C, Emlen D (2013) Evolution: making sense of life. Roberts, Greenwood Village
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
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.
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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
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