Female genotype affects male success in sperm competition

Abstract

The central question addressed by most studies of sperm competition is:`what determines which male's sperm are used at fertilization?' Empirical and theoretical studies that address this question have traditionally focused on adaptations which enhance male fertilization success while treating the female as a receptacle in which sperm competition is played out. Here we provide evidence which suggests that female genotype strongly in£uences the outcome of sperm competition. When the sperm of two males are in competition the proportion of o¡spring fathered by the second male to mate (P 2 ) was found to be highly repeatable only if the male pair were mated to three di¡erent, but genetically similar females (full-sisters to each other; unrelated to either of the males). In contrast, if a male pair were mated to three females that were unrelated then P 2 was either non-repeatable or marginally repeatable. We also show that male success in sperm competition is determined, to a large extent, by gamete and/or male^female compatibility. This conclusion is derived from the observation that P 2 was repeatable among full-sisters mated to di¡erent, yet genetically similar male pairings, whilst P 2 was non-repeatable among full-sisters mated to di¡erent, genetically distinct male pairings.

Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy

“…The incapacity of females to discriminate against related mates at the pre-copulatory level [39,43,44] and to avoid unwanted copulations [47,68], and the numerous fitness costs of inbreeding demonstrated in this species [14,35 -38,69], has probably promoted the evolution of a purely post-copulatory mechanism of cryptic female choice favouring fertilizations by unrelated males in the guppy. Our results, coupled with previous evidence that reports fertilization biases in favour of unrelated or genetically dissimilar males in other species [6][7][8][9][10][11][12][13], underscore the importance of post-copulatory inbreeding avoidance as an evolutionary force promoting polyandry.…”

“…It has been suggested that female multiple mating (polyandry) may have evolved as an inbreeding avoidance strategy mediated by post-copulatory mechanisms such as sperm-egg or sperm-female environment interactions [3][4][5], which could bias paternity towards unrelated or genetically compatible mates and hence reduce the costs of inbreeding. While growing evidence suggests that the genetic relatedness (or genetic similarity) between mating partners is associated with competitive fertilization success [6][7][8][9][10][11][12][13][14]although not always in the predicted direction (i.e. fertilization success biased in favour of males that are more genetically similar to the female [15][16][17][18])-most of these studies cannot exclude the influence of pre-copulatory mate choice or behavioural control of post-copulatory processes, which could bias fertilization success towards unrelated mates.…”

Cryptic Female Choice: Criteria for Establishing Female Sperm Choice

“…Eberhard (1996, p. 6) interpreted this as evidence for the preferential use by females of sperm from males with longer flagella. However, there are alternative explanations: males with a longer flagellum may simply be more efficient at getting their sperm to the best place to achieve fertilization and/ Wilson et al (1997) I Also referred to as Scathophaga (see Ward 1993Ward , 1997). …”

Distinguishing Between Female Sperm Choice Versus Male Sperm Competition: A Comment on Birkhead

“…If female sperm choice is a mechanism to avoid the negative effects of inbreeding (as the studies reviewed in Birkhead 1998 suggest), one could perform P 2 -experiments using groups of related versus unrelated females. Such an example is provided by Wilson et al (1997) and discussed in Birkhead (1998). A recent study on decorated field crickets (Gryllodes supplicans) used a different approach (Stockley 1999).…”

“…In the first study, Wilson et al (1997) took advantage of familial relatedness to partition sources of variation in P 2 in the cowpea weevil, Callosobruchus maculatus. This work is described in detail by Birkhead (1998) and by Telford and Jennions (1998).…”