Evolution of Ejaculates: Patterns of Phenotypic and Genotypic Variation and Condition Dependence in Sperm Competition Traits

Abstract

Sperm competition is widely recognized as a potent force in evolution, influencing male behavior, morphology, and physiology. Recent game theory analyses have examined how sperm competition can influence the evolution of ejaculate expenditure by males and the morphology of sperm contained within ejaculates. Theoretical analyses rest on the assumption that there is sufficient genetic variance in traits important in sperm competition to allow evolving populations to move to the evolutionarily stable equilibrium. Moreover, patterns of genotypic variation can provide valuable insight into the nature of selection currently acting on traits. However, our knowledge of genetic variance underlying traits important in sperm competition is limited. Here we examine patterns of phenotypic and genotypic variation in four sperm competition traits in the dung beetle Onthophagus taurus. Testis weight, ejaculate volume, and copula duration were found to have high coefficients of additive genetic variation (CV(A)S), which is characteristic of fitness traits and traits subject to sexual selection. Heritabilities were high, and there was some evidence for Y-linked inheritance in testis weight. In contrast, sperm length had a low CV(A), which is characteristic of traits subject to stabilizing selection. Nevertheless, there was little residual variance so that the heritability of sperm length exceeded 1.0. Such a pattern is consistent with Y-linked inheritance in sperm length. Interestingly, we found that testis weight and sperm length were genetically correlated with heritable male condition. This finding holds important implications for potential indirect benefits associated with the evolution of polyandry.

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

“…The heritability of spermatheca shape was considerably less than spermatheca size (Table 2). Sperm length also exhibited significant variance due to sires (27). Restricted maximum likelihood methods returned estimates of genetic variance and heritability consistent with our previous ANOVA approach (27) ( Table 2).…”

“…Previously, we found male condition in O. taurus to be heritable and genetically correlated with sperm length; males of high condition produce shorter sperm, suggesting that short sperm may be costly to produce (27). Thus, the costs of producing shorter sperm may counter the continued reduction in sperm length imposed by postcopulatory female preferences.…”

“…We found significant levels of additive genetic variation in sperm length and the high heritability for this trait that is necessary for a sexually selected sperm process. Moreover, we found significant additive genetic variation in male condition (26) and strong genetic covariance between male condition and sperm length; males in high condition produced shorter sperm (27). These patterns of genetic (co)variance are necessary for viability indicator and/or sexy son processes and could provide an avenue for postcopulatory sexual selection in this beetle; females that selectively fertilize their eggs using short sperm could produce offspring of greater condition because of the genetic covariances between these traits (the good-sperm process) and sons with short sperm who would be more successful in sperm competition (the sexy-sperm process) (27).…”

“…Moreover, we found significant additive genetic variation in male condition (26) and strong genetic covariance between male condition and sperm length; males in high condition produced shorter sperm (27). These patterns of genetic (co)variance are necessary for viability indicator and/or sexy son processes and could provide an avenue for postcopulatory sexual selection in this beetle; females that selectively fertilize their eggs using short sperm could produce offspring of greater condition because of the genetic covariances between these traits (the good-sperm process) and sons with short sperm who would be more successful in sperm competition (the sexy-sperm process) (27). García-González and Simmons (28) have recently shown that short sperm do have a competitive fertilization advantage and that this advantage depends on the size of the female's sperm storage organ, the spermatheca.…”

“…For these dams the numbers of sons ranged from four to six (upper and lower 95%: four and five) and the number of daughters from one to nine (4.5 and five). Although the quantitative genetic analysis of sperm length has been published previously (27), we present these data again here both for completeness and because we use different methods for extracting variance components and the calculation of standard errors.…”