The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.
Over the past fifty years, the conceptual framework of post-copulatory sexual selection has been well developed. When a female is polyandrous, there is a potential for the sperm of several males to compete for fertilizations of her eggs (sperm competition), and for the female to exert some choice over which sperm will fertilize her eggs (cryptic female choice). Parker 1970, a review of sperm competition in insects, stimulated the development of sperm competition theory. Eberhard 1996, a book on cryptic female choice, underscores the diversity of mechanisms that can allow polyandrous females to choose sperm from a particular male to fertilize their eggs and launched the field of cryptic female choice. Much discussion and experimentation has centered on how to disentangle sperm competition from cryptic female choice. Simmons, et al. 1996 provides a rare example where cryptic female choice can be eliminated as a factor influencing paternity, and therefore the role of sperm competition is clear. Birkhead and Pizzari 2002 provides a comprehensive examination of both processes. Ball and Parker 2003 uses game theory to model the actions of multiple mechanisms of post-copulatory selection: sperm competition, female use of sperms and sexual conflict. Birkhead and Kappeler 2004 compares post-copulatory sexual selection in birds and primates to explore commonalities and differences related to diverse life histories and mating systems. Eberhard 2009 examines how post-copulatory sexual selection has progressed over the past few decades and points out that several mechanisms of sperm competition and cryptic female choice were studied independently of sexual selection theory until recently. Birkhead 2010 dives into the history of the post-copulatory sexual selection and identifies major turning points in the field. Birkhead 2000 presents the main principles of post-copulatory sexual selection in a book written for the general public.
Ball, Michael A., and Geoff A. Parker. 2003. Sperm competition games: Sperm selection by females. Journal of Theoretical Biology 224.1: 27–42.
Game theory modeling of sperm allocation and potential evolutionary stable strategies that incorporate sperm competition, cryptic female choice, and sexual conflict. Two models are described in depth that focus on favored and unfavored males, in addition to the associated costs for each sex (e.g., reduced fecundity, reduced mating rates).
Birkhead, Tim. 2000. Promiscuity: An evolutionary history of sperm competition. Cambridge, MA: Harvard Univ. Press.
The topic of post-copulatory sexual selection is presented in a clear and well-organized manner that is easily accessible to the general public.
Birkhead, Tim R. 2010. How stupid to not have thought of that: Post-copulatory sexual selection. Journal of Zoology 281.2: 78–93.
The theory of post-copulatory sexual selection is reviewed, with historical and contemporary accounts of key pioneers in biology (e.g., Darwin, Parker, Eberhard), their major contributions relative to post-copulatory sexual selection, and important scientific events.
Birkhead, Tim R., and Peter M. Kappeler. 2004. Post-copulatory sexual selection in birds and primates. In Sexual selection in primates: New and comparative perspectives. Edited by Peter M. Kappeler and Carel P. van Schaik, 151–174. Cambridge, UK: Cambridge Univ. Press.
The mechanisms and consequences of post-copulatory sexual selection are reviewed in birds and primates, two groups that differ dramatically in their reproductive strategies and mating systems. Behavioral and morphological adaptations are compared. Convergent evolution is attributed to shaping similarities in post-copulatory sexual selection in these groups.
Birkhead, Tim R., and Tommaso Pizzari. 2002. Evolution of sex: Postcopulatory sexual selection. Nature Reviews Genetics 3.4: 262–273.
The theory and predictions of sperm competition and cryptic female choice (directional and nondirectional) are reviewed, with examples of how these mechanisms of post-copulatory sexual selection are mediated across a broad range of taxa, and how they often result in sexual conflict. The relationship between pre- and post-copulatory selection, the integration between different post-copulatory mechanisms, and the rate of evolutionary change are discussed as major unresolved issues. Suggested areas of future research include the use of genetic and molecular tools to examine the genetic basis of post-copulatory traits.
Eberhard, William G. 1996. Female control: Sexual selection by cryptic female choice. Princeton, NJ: Princeton Univ. Press.
This seminal book was a catalyst for interest in cryptic female choice that uses a wide range of taxa (especially insects) to illustrate different mechanisms by which females can bias paternity during and after copulation. The importance of cryptic female choice in the process of sexual selection is underscored, with a multitude of examples to demonstrate the likely prevalence of the mechanism.
Eberhard, William G. 2009. Postcopulatory sexual selection: Darwin’s omission and its consequences. Proceedings of the National Academy of Sciences of the United States of America 106.S1: 10025–10032.
Post-copulatory sexual selection (sperm competition, cryptic female choice, and sexually antagonistic coevolution) is reviewed. Unusual and rapidly divergent phenomena (e.g., the elaborate structure of male genitalia), the physiological effects of seminal fluids on female reproductive processes, the occurrence of courtship behavior after initiation of copulation, and the complexity of interactions between gametes in plants are highlighted.
Parker, Geoff A. 1970. Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45.4: 525–567.
This seminal paper launched the development of the field of post-copulatory sexual selection, particularly sperm competition. Parker predicted that when females mate with different males, each male would benefit by simultaneously eliminating rival sperm from previous female matings, as well as from evolving traits to protect their own sperm from such elimination by rivals. An examination of the outcome of multiple mating in several insects supported the importance of sperm competition.
Simmons, Leigh W., Paula Stockley, Rebecca L. Jackson, and Geoff A. Parker. 1996. Sperm competition or sperm selection: No evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria. Behavioral Ecology and Sociobiology 38:199–206.
It can be challenging to disentangle the roles of sperm competition and cryptic female choice, but an experimental approach in yellow dung flies demonstrated that despite an apparent advantage of large size on paternity, controlling for body size on sperm transfer and displacement eliminated the large male advantage. Therefore, traits under sperm competition influenced paternity more than an apparent female preference for large body size. The importance of controlling for male effects before drawing conclusions about cryptic female choice is underscored.
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