Rapid Evolution of Lifespan in a Novel Environment: Sex-Specific Responses and Underlying Genetic Architecture

Abstract

Animal lifespans can vary substantially among closely related species and even among conspecific populations, but it is often difficult to identify environmental and genetic factors producing such variation. We used experimental evolution to examine how transfer to a novel environment affects adult lifespan and rates of senescence in a seed-feeding beetle. Three replicate lines of Callosobruchus maculatus (F.) were switched to a new host plant (cowpea), and each evolved shorter adult lifespans compared to a line maintained on the ancestral host (mung bean). However, the evolution of lifespan differed between the sexes; female lifespan was reduced by ~11% in all cowpea replicates, whereas male lifespan decreased by an average of only 5.6% and the magnitude of the reduction varied among replicates. Reduced lifespan in lines switched to cowpea mirrored the shorter lifespan observed in a separate population chronically associated with cowpea. We then performed crosses between the mung bean and cowpea lines to estimate the genetic architecture underlying the rapid evolution of a shorter lifespan on cowpea. Dominance (overdominance) contributed substantially to the difference between the cowpea and mung bean lines for female lifespan but not for male lifespan. However, details of the genetic architecture varied among the three replicate crosses, so that the convergent evolution of shorter female lifespan in the different cowpea lines did not arise from identical allelic substitutions. Our study demonstrates that insect lifespan can be predictably modified by a switch to a novel host plant, that both the magnitude of this response and its underlying genetic architecture can be sex-specific, and that convergent evolution of a complex trait such as lifespan can arise from different genetic mechanisms.