Abstract
Cryptic female choice (CFC) does not necessarily involve discriminative responses in the female nervous system to sperm from multiple mates. Even without any active sperm-choice mechanisms, polyandrous females can gain genetic benefits by having an arena in which genetically superior sperm are “automatically” sorted. In this chapter, possible mechanisms in this CFC category, termed “indirect CFC ,” are reviewed. A simple theoretical model is developed to examine the hypothesis that females obtain genetic benefits by allowing only partial displacement of stored sperm by subsequent mates. The model predicts that such restricted sperm displacement automatically grants genetic benefits when genetically superior males copulate more times per encounter with the female than less fit males. The promiscuous earwig species, Euborellia plebeja , provides an empirical example of this type of indirect CFC. The elongated female sperm-storage organs allow only partial removal and displacement of stored sperm by shorter male genitalia, resulting in a 20 % gain in paternity per mating. In staged mating trials, large males dominated male–male competition for burrows housing females, resulting in a significant increase in paternity by repeated matings with the same female. A numerical simulation based on this mating pattern showed that restricted sperm displacement (~20 % per mating) is optimal for females to accumulate sperm from larger males. Given that male body size is heritable, females were estimated to gain a 1.4 % increase in their sons’ mating success as a genetic benefit. Advantages and disadvantages of indirect CFC are discussed and compared with precopulatory mate choice and direct CFC.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Arnqvist G, Rowe L (1995) Sexual conflict and arms races between the sexes—a morphological adaptation for control of mating in a female insect. Proc R Soc Lond B 261:123–127
Baijal HN, Srivastava GK (1974) Notes on the biology of Euborellia plebeja (Dohrn). Indian J Entomol 36:23–27
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368
Briceño RD, Eberhard WG (1995) The functional morphology of male cerci and associated characters in 13 species of tropical earwigs (Dermaptera: Forficulidae, Labiidae, Carcinophoridae, Pygidicranidae). Smithsonian Contr Zool 555:1–63
Carayon J (1966) Paragenital system. In: Usinger RL (ed) Monograph of Cimicidae (Hemiptera–Heteroptera). Thomas Say Foundation, Entomological Society of America, College Park, Maryland, pp 81–167
Carré D, Sardet C (1984) Fertilization and early development in Beroe ovata. Dev Biol 105:188–195
Chargé R, Teplitsky C, Hingrat Y et al (2013) Quantitative genetics of sexual display, ejaculate quality and size in a lekking species. J Anim Ecol 82:399–407
Charlat S, Reuter M, Dyson EA et al (2007) Male-killing bacteria trigger a cycle of increasing male fatigue and female promiscuity. Curr Biol 17:273–277
Cordero A, Santolamazza-Carbone S, Utzeri C (1995) Male disturbance, repeated insemination and sperm competition in the damselfly Coenagrion scitulum (Zygoptera: Coenagrionidae). Anim Behav 47:437–449
Córdoba-Aguilar A, Uhia E, Cordero Rivera A (2003) Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals’ sperm displacement. J Zool 261:381–398
Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London
Dixson AF, Anderson MJ (2004) Effects of sexual selection upon sperm morphology and sexual skin morphology in primates. Int J Primatol 25:1159–1171
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Priceton University Press, Princeton
Eisenbach M, Giojalas LC (2006) Sperm guidance in mammals—an unpaved road to the egg. Nat Rev Mol Cell Biol 7:276–285
Evans JP, Sherman CDH (2013) Sexual selection and the evolution of egg-sperm interactions in broadcast-spawning invertebrates. Biol Bull 224:166–183
Fedorka KM, Mousseau TA (2002a) Tibial spur feeding in ground crickets: larger males contribute larger gifts (Orthoptera: Gryllidae). Florida Entomol 85:317–323
Fedorka KM, Mousseau TA (2002b) Material and genetic benefits of female multiple mating and polyandry. Anim Behav 64:361–367
Fedorka KM, Winterhalter WE, Mousseau TA (2007) The evolutionary genetics of sexual size dimorphism in the cricket Allonemobius socius. Heredity 99:218–223
García-González F (2004) Infertile matings and sperm competition: the effect of “nonsperm representations” on intraspecific variation in sperm precedence patterns. Am Nat 164:457–472
Griffin AS, Alonzo SH, Cornwallis CK (2013) Why do cuckolded males provide paternal care? PLoS Biol 11:e1001520
Gschwentner R, Tadler A (2000) Functional anatomy of the spermatheca and its duct in the seed bug Lygaeus simulans (Heteroptera : Lygaeidae). Eur J Entomol 97:305–312
Haas F, Kukalovà-Peck J (2001) Dermaptera hindwing structure and folding: new evidence for familial, ordinal and superordinal relationships within Neoptera (Insecta). Eur J Entomol 98:445–509
Haas F, Klass KD (2003) The basal phylogenetic relationships in the Dermaptera. In: Klass KD (ed) Proceedings of the first dresden meeting on insect phylogeny: phylogenetic relationships within the insect orders, dresden, september 19–21, 2003. Entomol Abhand 61:138–142
Haas F, Hwen JTC, Tang HB (2012) New evidence on the mechanics of wing unfolding in Dermaptera. Arthropod Syst Phylogeny 70:95–105
Harano T, Miyatake T (2009) Bidirectional selection for female propensity to remate in the bean beetle, Callosobruchus chinensis. Popul Ecol 51:89–98
Hartley IR, Davies NB, Hatchwell BJ et al (1995) The polygynandrous mating system of the alpine accentor, Prunella collaris. II: multiple paternity and parental effort. Anim Behav 49:789–803
Harvey PH, May RM (1989) Out for the sperm count. Nature 337:508–509
Höglund J, Alatalo RV (1995) Leks. Priceton University Press, Princeton
Kamimura Y (2000) Possible removal of rival sperm by the elongated genitalia of the earwig, Euborellia plebeja. Zool Sci 17:667–672
Kamimura Y (2003a) Effects of broken male intromittent organs on the sperm storage capacity of female earwigs, Euborellia plebeja. J Ethol 21:29–35
Kamimura Y (2003b) Effects of repeated mating and polyandry on the fecundity, fertility and maternal behaviour of female earwigs, Euborellia plebeja. Anim Behav 65:205–214
Kamimura Y (2004) Mating behaviour and insemination in Diplatys flavicollis, an earwig with double-barreled penises and a variable number of female sperm-storage organs. J Zool 262:37–46
Kamimura Y (2005) Last male paternity of Euborellia plebeja, an earwig with elongated genitalia and sperm removal behavior. J Ethol 23:35–41
Kamimura Y (2013) Promiscuity and elongated sperm storage organs work cooperatively as a cryptic female choice mechanism in an earwig. Anim Behav 85:377–383
Kamimura Y (2014) Pre- and postcopulatory sexual selection and the evolution of sexually dimorphic traits in earwigs (Dermaptera). Entomol Sci 17:139–166
Kamimura Y, Matsuo Y (2001) A “spare” compensates for the risk of destruction of the elongated penis of earwigs (Insecta: Dermaptera). Naturwissenschaften 88:468–471
Kamimura Y, Iwase R (2010) Evolutionary genetics of genital size and lateral asymmetry in the earwig Euborellia plebeja (Dermaptera: Anisolabididae). Biol J Linn Soc 101:103–112
Kamimura Y, Lee C-Y (2014a) Mating and genital coupling in the primitive earwig species Echinosoma denticulatum (Pygidicranidae): implications for genital evolution in dermapteran phylogeny. Arthropod Syst Phylogeny 72:11–21
Kamimura Y, Lee C-Y (2014b) Genital morphology and mating behaviour of Allostethus (Dermaptera), an earwig genus of enigmatic phylogenetic position. Arthropod Syst Phylogeny 72:331–343
Keller L, Reeve HK (1995) Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav 24:291–315
Kempenaers B, Verheyen GR, Van den Broeck M et al (1996) Extra-pair paternity results from female preference for high quality males in the blue tit. Nature 357:494–496
Klass K-D (2003) The female genitalic region in basal earwigs (Insecta: Dermaptera: Pygidicranidae s.l.). Entomol Abhand 61:173–225
van Lieshout E (2011) Male genital length and mating status differently affect mating behaviour in an earwig. Behav Ecol Sociobiol 65:149–156
van Lieshout E, Elgar MA (2011a) Longer exaggerated male genitalia confer defensive sperm-competitive benefits in an earwig. Evol Ecol 25:351–362
van Lieshout E, Elgar MA (2011b) Owner positional disadvantage in contests over mating prevents monopolization of females. Anim Behav 82:753–758
Lodesani M, Balduzzi D, Galli A (2004) A study on spermatozoa viability over time in honey bee (Apis mellifera ligustica) queen spermathecae. J Apicul Res 43:27–28
Lüpold S, Tomkins JL, Simmons LW et al (2014) Female monopolization mediates the relationship between pre- and postcopulatory sexual traits. Nat Commun 5:3184
Micholitsch T, Krugel P, Pass G (2000) Insemination and fertilization in the seed bug Lygaeus simulans (Heteroptera : Lygaeidae). Eur J Entomol 97:13–18
Parker GA (1990) Sperm competition games: raffles and roles. Proc R Soc B Biol Sci 242:120–126
Perry JC, Rowe L (2012) Sexual conflict and antagonistic coevolution across water strider populations. Evolution 66:544–557
Pizzari T, Birkhead TR (2000) Female feral fowl eject sperm of subdominant males. Nature 405:787–789
Popham EJ (2000) The geographical distribution of the Dermaptera (Insecta) with reference to continental drift. J Nat Hist 34:2007–2027
Requena GS, Alonzo SH (2014) Female sperm use and storage between fertilization events drive sperm competition and male ejaculate allocation. Evolution 68:3433–3444
Schneider K, Klass K-D (2013) The female genitalic region in Eudermaptera (Insecta: Dermaptera). Zool Anzeiger 252:183–203
Sheldon BC (2002) Relating paternity to paternal care. Phil Trans R Soc Lond Ser B 357:341–350
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton
Singh SR, Singh BN (2001) Female remating in Drosophila ananassae: bidirectional selection for remating speed. Behav Genet 31:361–370
Siva-Jothy MT, Tsubaki Y (1989) Variation in copulation duration in Mnais pruinosa pruinosa Selys (Odonata: Calopterygidae) 1: alternative mate-securing tactics and sperm precedence. Behav Ecol Sociobiol 24:39–45
Slatyer RA, Jennions MD, Backwell PRY (2012) Polyandry occurs because females initially trade sex for protection. Anim Behav 83:1203–1206
Smith SM (1988) Extra-pair copulations in the black-capped chickadee: the role of the female. Behaviour 107:15–23
South A, Lewis SM (2011) The influence of male ejaculate quantity on female fitness: a meta-analysis. Biol Rev 86:299–309
Srivastava GK (1999) On the higher classification of Anisolabididae (Insecta: Dermaptera) with check-list of genera. Rec Zool Surv India 97:73–100
Tadler A (1999) Selection of a conspicuous male genitalic trait in the seedbug Lygaeus simulans. Proc R Soc B Biol Sci 266:1773–1777
Tsuchiya K, Hayashi F (2010) Factors affecting sperm quality before and after mating of calopterygid damselflies. PLoS ONE 5:e9904
Wada T, Takegaki T, Mori T et al (2005) Sperm displacement behavior of the cuttlefish Sepia esculenta (Cephalopoda: Sepiidae). J Ethol 23:85–92
Wedell N, Gage MJG, Parker GA (2000) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320
Wiley RH, Poston J (1996) Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50:1371–1381
Yanagimachi R, Cherr G, Matsubara T et al (2013) Sperm attractant in the micropyle region of fish and insect eggs. Biol Rep 88:1–11
Yasui Y (1997) A ‘good-sperm’ model can explain the evolution of costly multiple mating by females. Am Nat 149:573–584
Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13:246–250
Yeates SE, Diamond SE, Einum S et al (2013) Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior. Evolution 67:3523–3536
Acknowledgments
I thank A. Aisenberg and A. Peretti for the invitation to write this chapter, and G.S. Requena and an anonymous reviewer for useful comments on a previous version of this manuscript. A theoretical model of this chapter (Sect. 10.3) was developed as part of my unpublished doctoral thesis. I am also grateful to T. Suzuki, T. Kusano, and F. Hayashi for their supervision during the study. Writing of this manuscript was supported in part by a Keio Gijuku Academic Development Fund grant from Keio University.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Kamimura, Y. (2015). What Is Indirect Cryptic Female Choice? Theoretical Considerations and an Example from a Promiscuous Earwig. In: Peretti, A., Aisenberg, A. (eds) Cryptic Female Choice in Arthropods. Springer, Cham. https://doi.org/10.1007/978-3-319-17894-3_10
Download citation
DOI: https://doi.org/10.1007/978-3-319-17894-3_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-17893-6
Online ISBN: 978-3-319-17894-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)