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 livebearing 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.

Population demography and heterozygosity–fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

“…Sperm head, tail and total lengths were all highly correlated and gave qualitatively similar results to one another in our subsequent analyses. Midpiece length was not highly correlated with the other measurements, corresponding to previous patterns reported for guppies (Evans, ). We therefore focus on midpiece and total length separately in our subsequent analyses (see Linear modelling ).…”

“…); consistent with the output of our interaction models, no consistent patterns are evident. We note that our models should not be considered as independent: guppies exhibit complex genetic covariance among sexual behaviours, ornamentation and ejaculate traits that could constrain how sexually selected traits respond to inbreeding (Evans, , ; see Discussion). Finally, simpler HFC models run for each population and trait separately indicated no overall patterns at the population or trait level; only a few statistically significant HFCs were detected (the 95% CI excluded zero for 9 of 241 models [3.73%]; Fig.…”

Postcopulatory inbreeding avoidance in guppies

“…Interestingly, however, the remaining sperm traits assessed in this study (sperm morphology and velocity) did not predict sperm competitiveness. This is surprising as sperm viability is negatively genetically correlated with sperm morphology (head, flagellum and total length) in the study population (Evans, ). Yet, our finding is partially in keeping with recent work on guppies and other poeciliid fishes that did not find an effect of sperm morphology and only weak effects of sperm swimming speed on competitive fertilization success (Gasparini et al ., ; Boschetto et al ., ; Smith, ).…”

Male sperm storage compromises sperm motility in guppies

“…By comparing old and young ejaculates within the same male, and hence accounting for inter-male variability in sperm traits [13,15], we found that old sperm exhibited impaired sperm velocity compared with young sperm. As we did not use natural matings to manipulate sperm ageing, we were able to disentangle the effects of sperm ageing per se from variance attributable to mating history and male-female social interactions.…”