Sexual selection in mosquito swarms: may the best man lose?

Abstract

One of the greatest paradoxes in evolutionary biology is the continued maintenance of genetic variation for phenotypic traits that appear to confer strong fitness advantages. Of these traits, body size is perhaps the one that has been most consistently linked to increased longevity and reproductive success in males. We investigated two hypotheses for how events occurring during mating in the mosquito Anopheles gambiae could impede directional selection on male body size: (1) whether male copulation probability is random with respect to body size in aerial swarms, and (2) whether large males are less competitive during mating than smaller, shorter-lived rivals. By manipulation of larval nutritional conditions (low, intermediate and high food allocation), we generated cohorts of male A. gambiae mosquitoes that differed in adult body size and energy reserves (body size and energy reserves being positively correlated with larval nutrition). When competing against one another in aerial swarms, males from the intermediate food treatment were six and two times more successful at acquiring mates than those from the high and low food treatments, respectively. The median survival of males from this most sexually competitive group was approximately 13% lower than that of the larger males with high larval nutrition. We conclude that phenotypic determinants of long-term survival and mating success may not be correlated in this system, and thus that stabilizing selection as well as environmental condition-dependent expression of traits could account for the maintenance of variation in male body size in this species and in other swarming insects.