Environmental effects on sex differences in the genetic load for adult lifespan in a seed-feeding beetle

Abstract

We have little understanding of how environmental conditions affect the expression of the genetic load for lifespan and adult mortality rates, or how this environmental dependence affect tests of models for the evolution of senescence. We use the seed-feeding beetle, Callosobruchus maculatus, as a model to explore how the inbreeding load (L) affecting adult lifespan varies with rearing conditions (diet and temperature), and how rearing conditions affect tests of the mutation accumulation model of senescence. When reared under benign conditions, there was a large sex difference in inbreeding depression (delta) and the inbreeding load (L=0.51-0.86 lethal equivalents per gamete for females L= approximately 0 for males). This sex difference in L was dependent on temperature, but not on rearing host or heat shock. At both high and low temperatures (relative to intermediate temperature) L increased for males, and L converged for the sexes at low temperature (L=0.26-0.53 for both sexes). Correlations were small for L between pairs of temperatures, indicating that the genes responsible for the inbreeding load differed between temperatures. In contrast to predictions of the mutation accumulation model of senescence, the age-specific inbreeding load for the adult mortality rate (L(u(t))) did not increase with age in any rearing environment. The genetic load underlying lifespan and adult mortality rates, and large sex differences in the genetic load, is highly dependent on environmental conditions. Estimating the genetic load in benign laboratory environments may be insufficient to predict the genetics underlying lifespan variation in nature where environmental variation is the norm.