Cryptic Female Choice

by

Hanne Løvlie

• LAST REVIEWED: 31 March 2016
• LAST MODIFIED: 31 March 2016
• DOI: 10.1093/obo/9780199941728-0071

Introduction

Sexual selection (see the Oxford Bibliographies article “Sexual Selection”) is a powerful evolutionary force, selecting for traits that increase the reproductive success of individuals. Before copulation, sexual selection can occur through intrasexual selection, typically observed as competition among individuals of the same sex for access to mating partners of the other sex (see Oxford Bibliographies article on Evolutionary Biology “Male-Male Competition”), and intersexual selection, observed as (typically female) mate choice (see Oxford Bibliographies article on Evolutionary Biology “Mate Choice”). When females are sexually promiscuous and mate with multiple males (which is more the rule than the exception in the animal kingdom), these two processes have the potential to continue also after copulation: intrasexual selection as sperm competition (Oxford Bibliographies article on Evolutionary Biology “Sperm Competition”), and intersexual selection as cryptic female choice. The term cryptic is applied because this form of female choice can be hard to observe (e.g., when it occurs inside the female reproductive tract) and hard to quantify with classical measures of reproductive success (e.g., mating success). In addition, this form of female choice is hard to disentangle from other episodes of sexual selection (see below). The framework used to understand female choice occurring after (or sometimes during) copulation is currently somewhat divergent, since some authors adopt a very broad definition of cryptic female choice, while others apply a more conservative definition (see discussion of this under Definition and History). Cryptic female choice is a relatively young research topic (it first started properly after the publication of Eberhard’s seminal book Female Control: Sexual Selection by Cryptic Female Choice [Eberhard 1996, cited under General Overviews] in 1996). It was realized early on in the history of the field that a broad range of mechanisms across a variety of species exist through which females can potentially bias the outcome of a copulation (e.g., ejaculate ejection, differential sperm storage, sperm choice—see section Mechanisms and Processes Used as Cryptic Female Choice). As a consequence, measures of precopulatory processes or sperm competition can be misleading in species with cryptic female choice, due to female postcopulatory influences on fertilization. Yet, although there is no doubt that females have great potential to bias paternity at the postcopulatory stage, cryptic female choice is the least studied of the processes through which sexual selection can occur (e.g., compared to sperm competition, or male-male competition). This is probably because demonstration of cryptic female choice is notoriously difficult. It can be challenging to separate pre- from postcopulatory processes, the interaction of male adaptations to sperm competition and female influences on fertilization, and variation in differential embryo mortality from female-induced biases in paternity (see Potential Pitfalls in the Study of Cryptic Female Choice). The studies that have convincingly been able to separate these processes and demonstrate cryptic female choice are currently primarily from insect, bird, and externally fertilizing species (see Mechanisms and Processes Used as Cryptic Female Choice). I here present when we may expect to observe cryptic female choice, how females may benefit from cryptic female choice, some techniques that can be useful for studies of cryptic female choice, and some of the theoretical work that includes cryptic female choice.

General Overviews

The research field cryptic female choice originated during the early 1990s, with only a few papers published before then. Compared to other areas of sexual selection, there are relatively few books or review articles fully dedicated to cryptic female choice. However, there is one large exception to this, which is also the book that convincingly established cryptic female choice as an important component of sexual selection; Eberhard’s seminal Female Control: Sexual Selection by Cryptic Female Choice (Eberhard 1996). Eberhard presented numerous potential mechanisms by which females can conduct postcopulatory choice, ranging from female behavior during copulation to female physiology and morphology, to varying investment in offspring. Another important book is Birkhead and Møller 1998, which gives an excellent overview of postcopulatory sexual selection across a broad range of taxonomic groups. Although this book focuses on sperm competition, several chapters are of great relevance for cryptic female choice. Similarly, Birkhead, et al. 2009 gives an extensive treatment across the broad topic of sperm biology. Several chapters in this book are also of direct relevance for researchers interested in cryptic female choice. Additionally, Eberhard presented a short and updated paper in Eberhard 2009, which includes a list of a broad range of potential mechanisms under female control that could bias the outcome of a copulation. Of the relevant journal articles, Birkhead 1998 (cited under Potential Pitfalls in the Study of Cryptic Female Choice) and the replies published following it, particularly Pitnick and Brown 2000 and Birkhead 2000 (both under Potential Pitfalls in the Study of Cryptic Female Choice), which discuss how to demonstrate cryptic female choice, are key publications in the field. Due to the many and complex ways ejaculates and females, and sperm and eggs, can interact, Eberhard 1996 and Pitnick, et al. 2009 (cited under Definition and History) suggest that the dichotomy of sperm competition versus cryptic female choice may not be very useful, but to instead call the entirety “postcopulatory sexual selection.” This again highlights that separating cryptic female choice from other processes can be difficult, which in turn makes the study of cryptic female choice hard. A small number of excellent recent review papers summarize our understanding of postcopulatory sexual selection and incorporate cryptic female choice, including Birkhead and Pizzari 2002, Simmons 2001, Simmons 2005 (cited under Potential Pitfalls in the Study of Cryptic Female Choice), Andersson and Simmons 2006, Birkhead 2010 (cited under Definition and History), Parker and Birkhead 2013 (cited under Definition and History). Finally, Birkhead 2000 is a popular science book that presents scientifically accurate and entertaining examples of postcopulatory sexual selection (although mainly focusing on sperm competition).

• Andersson, M., and L. W. Simmons. 2006. Sexual selection and mate choice. Trends in Ecology and Evolution 21:296–302.

  DOI: 10.1016/j.tree.2006.03.015

  This is a review of studies on mate choice from the prior two decades (both empirical and theoretical), and also includes mate choice occurring after copulation.

• Birkhead, T. R. 2000. Promiscuity: An evolutionary history of sperm competition. Cambridge, MA: Harvard Univ. Press.

  An entertaining popular science book that presents sperm competition from an evolutionary perspective accessible to both researchers and the wider public.

• Birkhead, T. R., D. J. Hosken, and S. Pitnick, eds. 2009. Sperm biology: An evolutionary perspective. Amsterdam and London: Elsevier.

  The most recent and extensive overview of sperm competition and sperm biology. More relevant chapters with regards to cryptic female choice are Pitnick, et al. 2009 (cited under Mechanisms and Processes Used as Cryptic Female Choice); Karr, et al. 2009 (cited under Sperm-Egg Interactions); and Birkhead and Montgomerie 2009 (cited under Definition and History).

• Birkhead, T. R., and A. P. Møller, eds. 1998. Sperm competition and sexual selection. London: Academic Press.

  A brilliant book reviewing three decades of research on sperm competition in various taxa. Particularly relevant chapters for cryptic female choice are Parker on “Sperm Competition and the Evolution of Ejaculates” (Parker 1998, cited under Theoretical Models Including Cryptic Female Choice), Eberhard on “Female Roles in Sperm Competition,” Simmons and Siva-Jothy on “Sperm Competition in Insects,” Birkhead on “Sperm Competition in Birds,” and Birkhead and Møller’s concluding chapter on the various routes through which males and females can affect fitness.

• Birkhead, T. R., and T. Pizzari. 2002. Postcopulatory sexual selection. Nature Reviews: Genetics 3:262–273.

  DOI: 10.1038/nrg774

  This review provides a useful overview of postcopulatory sexual selection, including cryptic female choice.

• Eberhard, W. G. 1996. Female control: Sexual selection by cryptic female choice. Princeton, NJ: Princeton Univ. Press.

  The seminal monograph demonstrating that cryptic female choice can have important implications for sexual selection. Eberhard presents an extensive coverage of the many potential avenues through which females can bias paternity. Eberhard’s book is still the main, and so far only, book focusing entirely on cryptic female choice.

• Eberhard, W. 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.Suppl. 1: 10025–10032.

  DOI: 10.1073/pnas.0901217106

  This is a more recent summary of Eberhard’s view on postcopulatory sexual selection, including cryptic female choice. The paper includes a table listing a broad range of routes through which females can potentially bias the outcome of a copulation.

• Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton, NJ: Princeton Univ. Press.

  An extensive review of three decades of research on postcopulatory sexual selection (including cryptic female choice) in insects. Chapter 9, “Ejaculate Manipulation: Mechanisms of Female Choice,” is particularly relevant for researchers interested in cryptic female choice.