Maternal and Paternal Age Effects on Male Antler Flies: A Field Experiment.

AbstractIn many species, parental age at reproduction can influence offspring performance and life span, but the direction of these effects and the traits affected vary among studies. Data on parental age effects are still scarce in noncaptive populations, especially insects, despite species such as fruit flies being models in laboratory-based aging research. We performed a biologically relevant experimental manipulation of maternal and paternal age at reproduction of antler flies (Protopiophila litigata) in the laboratory and tracked the adult life span and reproductive success of their male offspring released in the wild. Increased paternal, but not maternal, age somewhat increased sons' adult life span, while parental ages did not influence sons' mating rate or reproductive senescence. Our results indicate that while parental age effects do exist in an insect in the field, they may be beneficial in such a short-lived animal, in contrast to results from most wild vertebrates and laboratory invertebrates.

Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild.

High-quality developmental environments often improve individual performance into adulthood, but allocating toward early life traits, such as growth, development rate and reproduction, may lead to trade-offs with late-life performance. It is, therefore, uncertain how a rich developmental environment will affect the ageing process (senescence), particularly in wild insects. To investigate the effects of early life environmental quality on insect life-history traits, including senescence, we reared larval antler flies (Protopiophila litigata) on four diets of varying nutrient concentration, then recorded survival and mating success of adult males released in the wild. Declining diet quality was associated with slower development, but had no effect on other life-history traits once development time was accounted for. Fast-developing males were larger and lived longer, but experienced more rapid senescence in survival and lower average mating rate compared to slow developers. Ultimately, larval diet, development time and body size did not predict lifetime mating success. Thus, a rich environment led to a mixture of apparent benefits and costs, mediated by development time. Our results indicate that 'silver spoon' effects can be complex and that development time mediates the response of adult life-history traits to early life environmental quality.

Competition for mates and the improvement of nonsexual fitness.

Competition for mates can be a major source of selection, not just on secondary sexual traits but across the genome. Mate competition strengthens selection on males via sexual selection, which typically favors healthy, vigorous individuals and, thus, all genetic variants that increase overall quality. However, recent studies suggest another major effect of mate competition that could influence genome-wide selection: Sexual harassment by males can drastically weaken selection on quality in females. Because of these conflicting effects, the net effect of mate competition is uncertain, although perhaps not entirely unpredictable. We propose that the environment in which mate competition occurs mediates the importance of sexual selection relative to sexual conflict and, hence, the net effect of mate competition on nonsexual fitness. To test this, we performed experimental evolution with 63 fruit fly populations adapting to novel larval conditions where each population was maintained with or without mate competition. In half the populations with mate competition, adults interacted in simple, high-density environments. In the remainder, adults interacted in more spatially complex environments in which male-induced harm is reduced. Populations evolving with mate competition in the complex environment adapted faster to novel larval environments than did populations evolving without mate competition or with mate competition in the simple environment. Moreover, mate competition in the complex environment caused a substantial reduction in inbreeding depression for egg-to-adult viability relative to the other two mating treatments. These results demonstrate that the mating environment has a substantial and predictable effect on nonsexual fitness through adaptation and purging.