Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies

Abstract

Ejaculates comprise multiple and potentially interacting traits that determine male fertility and sperm competitiveness. Consequently, selection on these traits is likely to be intense, but the efficacy of selection will depend critically on patterns of genetic variation and covariation underlying their expression. In this study, I provide a prospective quantitative genetic analysis of ejaculate traits in the guppy Poecilia reticulata, a highly promiscuous live-bearing fish. I used a standard paternal half-sibling breeding design to characterize patterns of genetic (co)variation in components of sperm length and in vitro sperm performance. All traits exhibited high levels of phenotypic and additive genetic variation, and in several cases, patterns of genetic variation was consistent with Y-linkage. There were also highly significant negative genetic correlations between the various measures of sperm length and sperm performance. In particular, the length of the sperm's midpiece was strongly, negatively and genetically correlated with sperm's swimming velocity-an important determinant of sperm competitiveness in this and other species. Other components of sperm length, including the flagellum and head, were independently and negatively genetically correlated with the proportion of live sperm in the ejaculate (sperm viability). Whether these relationships represent evolutionary trade-offs depends on the precise relationships between these traits and competitive fertilization rates, which have yet to be fully resolved in this (and indeed most) species. Nevertheless, these prospective analyses point to potential constraints on ejaculate evolution and may explain the high level of phenotypic variability in ejaculate traits in this species.