Quantitative genetic correlation between trait and preference supports a sexually selected sperm process

Abstract

Sperm show patterns of rapid and divergent evolution that are characteristic of sexual selection. Sperm competition has been proposed as an important selective agent in the evolution of sperm morphology. However, several comparative analyses have revealed evolutionary associations between sperm length and female reproductive tract morphology that suggest patterns of male-female coevolution. In the dung beetle Onthophagus taurus, males with short sperm have a fertilization advantage that depends on the size of the female's sperm storage organ, the spermatheca; large spermathecae select for short sperm. Sperm length is heritable and is genetically correlated with male condition. Here we report significant additive genetic variation and heritability for spermatheca size and genetic covariance between spermatheca size and sperm length predicted by both the ''goodsperm'' and ''sexy-sperm'' models of postcopulatory female preference. Our data thus provide quantitative genetic support for the role of a sexually selected sperm process in the evolutionary divergence of sperm morphology, in much the same manner as precopulatory female preferences drive the evolutionary divergence of male secondary sexual traits.male-female coevolution ͉ postcopulatory female choice ͉ sperm length F emale mating preferences are widely recognized as being responsible for the rapid and divergent evolution of male secondary sexual traits (1). Indicator or good gene models envisage genetic coupling between male sexual trait expression and offspring fitness, so that females with a preference for male traits produce offspring of greater viability (2). Once a preference becomes established, females choosing males with elaborate secondary sexual traits will produce sons that carry alleles for the trait and daughters that carry alleles for the preference, generating genetic coupling that will drive self-reinforcing coevolution of both trait and preference because of the mating advantage to males with the trait. Thus, the original viability benefits associated with the preference can be undermined by a runaway Fisherian sexy sons process (2). Analogous models have been proposed for postcopulatory female preferences (3). ''Good-sperm'' models predict positive genetic associations between a male's sperm competitiveness and the general viability of his offspring (4), whereas ''sexy-sperm'' models predict that multiply mating females produce sons successful in sperm competition and daughters that incite sperm competition through multiple mating (5, 6). As with precopulatory processes, postcopulatory models predict that the trait in males that determines fertilization success will become genetically coupled with the mechanism by which females bias sperm use toward preferred males (7).Although spermatozoa are well known for their rapid and divergent morphological variation (8, 9), little is known of the selective processes that drive sperm evolution. Patterns of divergent evolution are characteristic of strong sexual selection, and researchers have sugges...

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

“…Our limited knowledge suggests that female reproductive tracts undergo rapid evolutionary diversification, with important implications for the intensity of sexual selection generated on males in general and on the form and function of numerous ejaculate traits in particular (Swanson et al 2001;Miller and Pitnick 2002;Higginson et al 2012aHigginson et al , 2012b. Important advances in postcopulatory sexual selection theory are likely to come from research into the selective causes of female reproductive tract divergence and addressing whether the same models for the evolution of premating female preferences (Andersson 1994) are sufficient to explain divergence in female tract traits functioning as the proximate basis of sperm choice (e.g., Curtsinger 1991; Keller and Reeve 1995;Simmons and Kotiaho 2007).…”

Testing the fisherian mechanism: examining the genetic correlation between male song and female response in waxmoths

“…Among the various researchers who have measured levels of genetic covariance between signal and preference traits, some have reported significant covariance (Bakker 1993;Houde 1994;Wilkinson and Reillo 1994;Simmons and Kotiaho 2007) while others, particularly in recent years, have noted its absence (Löfstedt et al 1989;Breden and Hornaday 1994;Morris et al 1996;Muhlhauser and Blanckenhorn 2004;Ritchie et al 2005;Qvarnström et al 2006;Allison et al 2008; also see Blows 1999, who reports initial positive and final negative results in the course of an experimental evolution study). In general, these studies have largely ignored the potential influences that environmental conditions (see Sgrò and Hoffmann 2004) and gene flow may exert on signal/preference covariance.…”

Condition-dependent ejaculate size and composition in a ladybird beetle

“…Following a series of environmental manipulations of condition, there is now considerable empirical evidence for condition dependence in several types of sexually selected traits, including secondary sexual morphology, ornaments and pigmentation, and acoustic signals (Andersson 1994;Cotton et al 2004 and references therein; Bonduriansky & Rowe 2005;Punzalan et al 2008). Recent evidence suggests that male ejaculates are also sexually selected (Eberhard & Cordero 1995;Ramm et al 2007;Simmons & Kotiaho 2007;Martin-Coello et al 2009;Wigby et al 2009) and costly (e.g. Dewsbury 1982).…”