The coevolutionary dynamics of cryptic female choice

Abstract In contrast to sexual selection on traits that affect interactions between the sexes before mating, little theoretical research has focused on the coevolution of postmating traits via cryptic female choice (when females bias fertilization toward specific males). We used simulation models to ask (a) whether and, if so, how nondirectional cryptic female choice (female-by-male interactions in fertilization success) causes deviations from models that focus exclusively on male-mediated postmating processes, and (b) how the risk of sperm competition, the strength of cryptic female choice, and tradeoffs between sperm number and sperm traits interact to influence the coevolutionary dynamics between cryptic female choice and sperm traits. We found that incorporating cryptic female choice can result in males investing much less in their ejaculates than predicted by models with sperm competition only. We also found that cryptic female choice resulted in the evolution of genetic correlations between cryptic female choice and sperm traits, even when the strength of cryptic female choice was weak, and the risk of sperm competition was low. This suggests that cryptic female choice may be important even in systems with low multiple mating. These genetic correlations increased with the risk of sperm competition and as the strength of cryptic female choice increased. When the strength of cryptic female choice and risk of sperm competition was high, extreme codivergence of sperm traits and cryptic female choice preference occurred even when the sperm trait traded off with sperm number. We also found that male traits lagged behind the evolution of female traits; this lag decreased with increasing strength of cryptic female choice and risk of sperm competition. Overall, our results suggest that cryptic female choice deserves more attention theoretically and may be driving trait evolution in ways just beginning to be explored.

[1]  M. Ah-King,et al.  The history of sexual selection research provides insights as to why females are still understudied , 2022, Nature Communications.

[2]  Zelealem B. Yilma,et al.  Selection on sperm size in response to promiscuity and variation in female sperm storage organs , 2022, bioRxiv.

[3]  D. Shuker,et al.  The definition of sexual selection , 2021, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[4]  Catherine A. Rushworth,et al.  Conflict over fertilization underlies the transient evolution of reinforcement , 2020, bioRxiv.

[5]  J. Evans,et al.  The role of female reproductive fluid in sperm competition , 2020, Philosophical Transactions of the Royal Society B.

[6]  J. Belote,et al.  How female × male and male × male interactions influence competitive fertilization in Drosophila melanogaster , 2020, Evolution letters.

[7]  J. Fitzpatrick,et al.  Chemical signals from eggs facilitate cryptic female choice in humans , 2020, Proceedings of the Royal Society B.

[8]  G. Machado,et al.  Within‐population variation in female mating preference affects the opportunity for sexual selection and the evolution of male traits, but things are not as simple as expected , 2020, Journal of evolutionary biology.

[9]  J. Henshaw,et al.  Fisher's lost model of runaway sexual selection , 2019, Evolution; international journal of organic evolution.

[10]  Kohske Takahashi,et al.  Welcome to the Tidyverse , 2019, J. Open Source Softw..

[11]  M. Wolfner,et al.  Post‐ejaculatory modifications to sperm (PEMS) , 2019, Biological reviews of the Cambridge Philosophical Society.

[12]  C. Gasparini,et al.  Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish , 2019, Behavioral Ecology.

[13]  D. Irwin Assortative mating in hybrid zones is remarkably ineffective in promoting speciation , 2019, bioRxiv.

[14]  L. Simmons,et al.  Female genitalia can evolve more rapidly and divergently than male genitalia , 2019, Nature Communications.

[15]  G. Parker,et al.  Endless forms of sexual selection , 2019, PeerJ.

[16]  S. Pitnick,et al.  Sperm form and function: what do we know about the role of sexual selection? , 2018, Reproduction.

[17]  J. Evans,et al.  Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post‐copulatory isolation between two guppy populations , 2018, Journal of evolutionary biology.

[18]  M. Servedio,et al.  The Role of Sexual Selection in Local Adaptation and Speciation , 2017 .

[19]  R. C. Firman,et al.  Postmating Female Control: 20 Years of Cryptic Female Choice , 2017, Trends in ecology & evolution.

[20]  Jussi Lehtonen The Lambert W function in ecological and evolutionary models , 2016 .

[21]  J. Belote,et al.  How sexual selection can drive the evolution of costly sperm ornamentation , 2016, Nature.

[22]  I. Fleming,et al.  Inter-population ovarian fluid variation differentially modulates sperm motility in Atlantic cod Gadus morhua. , 2015, Journal of fish biology.

[23]  R. Prum,et al.  Mechanisms and Evidence of Genital Coevolution: The Roles of Natural Selection, Mate Choice, and Sexual Conflict. , 2015, Cold Spring Harbor perspectives in biology.

[24]  J. Fitzpatrick,et al.  Sexual selection and the evolution of sperm quality. , 2014, Molecular human reproduction.

[25]  G. Bocedi,et al.  Evolution of female multiple mating: A quantitative model of the “sexually selected sperm” hypothesis , 2014, Evolution; international journal of organic evolution.

[26]  Alan Edelman,et al.  Julia: A Fresh Approach to Numerical Computing , 2014, SIAM Rev..

[27]  Michael D. Martin,et al.  Mutation-order divergence by sexual selection: diversification of sexual signals in similar environments as a first step in speciation. , 2014, Ecology letters.

[28]  J. Evans,et al.  Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate , 2014, Proceedings of the Royal Society B: Biological Sciences.

[29]  R. Bürger,et al.  The counterintuitive role of sexual selection in species maintenance and speciation , 2014, Proceedings of the National Academy of Sciences.

[30]  A. Møller,et al.  Do male secondary sexual characters signal ejaculate quality? A meta‐analysis , 2013, Biological reviews of the Cambridge Philosophical Society.

[31]  J. Evans,et al.  Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia , 2013, Proceedings of the Royal Society B: Biological Sciences.

[32]  T. Laskemoen,et al.  Rapid sperm evolution in the bluethroat (Luscinia svecica) subspecies complex , 2013, Behavioral Ecology and Sociobiology.

[33]  F. Weissing,et al.  A Guide to Sexual Selection Theory , 2012 .

[34]  K. A. Segraves,et al.  Female reproductive tract form drives the evolution of complex sperm morphology , 2012, Proceedings of the National Academy of Sciences.

[35]  G. Parker,et al.  Resolving variation in the reproductive tradeoff between sperm size and number , 2011, Proceedings of the National Academy of Sciences.

[36]  G. Parker,et al.  Sperm competition and ejaculate economics , 2010, Biological reviews of the Cambridge Philosophical Society.

[37]  G. Parker,et al.  Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. , 2010, Journal of theoretical biology.

[38]  R. Montgomerie,et al.  A mechanism for cryptic female choice in chinook salmon , 2008 .

[39]  S. Palumbi,et al.  Intraspecific divergence in sperm morphology of the green sea urchin, Strongylocentrotus droebachiensis: implications for selection in broadcast spawners , 2008, BMC Evolutionary Biology.

[40]  S. J. Arnold,et al.  Estimating Nonlinear Selection Gradients Using Quadratic Regression Coefficients: Double Or Nothing? , 2008, Evolution; international journal of organic evolution.

[41]  L. Simmons,et al.  Quantitative genetic correlation between trait and preference supports a sexually selected sperm process , 2007, Proceedings of the National Academy of Sciences.

[42]  S. Pitnick,et al.  Complex interactions with females and rival males limit the evolution of sperm offence and defence , 2007, Proceedings of the Royal Society B: Biological Sciences.

[43]  P. D. Lorch,et al.  The evolution of conspecific gamete precedence and its effect on reinforcement , 2007, Journal of evolutionary biology.

[44]  I. Folstad,et al.  Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus) , 2005, Behavioral Ecology and Sociobiology.

[45]  G. Parker,et al.  Sperm competition games: sperm selection by females. , 2003, Journal of theoretical biology.

[46]  T. Markow,et al.  Ejaculate-female coevolution in Drosophila mojavensis , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  S. Pitnick,et al.  Sperm-Female Coevolution in Drosophila , 2002, Science.

[48]  T. Birkhead,et al.  Evolution of sex: Postcopulatory sexual selection , 2002, Nature Reviews Genetics.

[49]  N. Barton,et al.  Theory and speciation. , 2001, Trends in ecology & evolution.

[50]  D. Levitan Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  A. Clark,et al.  Female x male interactions in Drosophila sperm competition. , 1999, Science.

[52]  R. Montgomerie,et al.  THE EVOLUTION OF SPERM SIZE IN BIRDS , 1997, Evolution; international journal of organic evolution.

[53]  M. Petrie,et al.  VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES , 1997, Biological reviews of the Cambridge Philosophical Society.

[54]  Y. Yasui A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females , 1997, The American Naturalist.

[55]  L. Keller,et al.  Why Do Females Mate with Multiple Males? The Sexually Selected Sperm Hypothesis , 1995 .

[56]  G. Parker Sperm competition games: sperm size and sperm number under adult control , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  Louise S. Mead,et al.  Quantitative genetic models of sexual selection. , 1985, Trends in ecology & evolution.

[58]  R. Thornhill Cryptic Female Choice and Its Implications in the Scorpionfly Harpobittacus nigriceps , 1983, The American Naturalist.

[59]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

[60]  M. Kirkpatrick SEXUAL SELECTION AND THE EVOLUTION OF FEMALE CHOICE , 1982, Evolution; international journal of organic evolution.

[61]  R. Lande Models of speciation by sexual selection on polygenic traits. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[62]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[63]  M. Wolfner,et al.  Ejaculate–female and sperm–female interactions , 2009 .

[64]  T. Birkhead,et al.  Sperm morphological diversity , 2009 .

[65]  D. J. Howard,et al.  Sperm and speciation , 2009 .

[66]  R. Snook Sperm in competition: not playing by the numbers. , 2005, Trends in ecology & evolution.

[67]  G. Parker 1 – Sperm Competition and the Evolution of Ejaculates: Towards a Theory Base , 1998 .

[68]  M. Kirkpatrick,et al.  The evolution of mating preferences and the paradox of the lek , 1991, Nature.

[69]  G. Parker,et al.  SPERM COMPETITION AND ITS EVOLUTIONARY CONSEQUENCES IN THE INSECTS , 1970 .