Mutation accumulation affects male virility in Drosophila selected for later reproduction

Abstract

An intensive study of longevity, female fecundity, and male reproductive behavior in Drosophila melanogaster was undertaken in order to establish whether late-life fitness characters in short-lived populations might be affected by the increase in deleterious alleles due to random genetic drift. We also sought to determine whether selection for late-life fertility could eliminate alleles that produce a decline in later fitness components in short-lived populations, as predicted by the mutation accumulation hypothesis for the evolution of aging. These experiments employed long-lived (O) populations, short-lived (B) populations, and hybrids made from crosses of independent lines from within the O and B populations. No detectable longevity differences were seen between hybrid B males and females and purebred B males and females. Reproduction in aged B purebred females was significantly less than in hybrid females at 3 wk of age only. A full diallel cross of the five replicate B lines showed a steady increase in hybrid male reproductive performance after the first week of adult life, relative to the parental lines. A full diallel cross of the five replicate O lines revealed no significant increase in hybrid O age-specific male reproductive success compared with the purebred O lines when assayed over the first 5 wk of adult life. The results on male reproductive behavior are consistent with the idea that relaxed age-specific selection in the B populations has been accompanied by an increase in deleterious, recessive traits that exhibit age-specific expression. Consequently, we conclude that a mutation accumulation process has been at least partly responsible for the age-specific decline in male B virility relative to that of the O populations.