Developmental plasticity for male secondary sexual traits in a group of polyphenic tropical butterflies

Abstract

Many organisms alter their investment in secondary sexual traits to optimise the fitness tradeoff between reproduction and survival. Though seasonal variation in the expression of sexual traits is evident (e.g. conspicuous breeding plumage in birds), little attention has been given to short-lived organisms that inhabit relatively stable environments throughout their own lifetime but are exposed to strong environmental variation across generations. Some insects have evolved seasonal polyphenism to cope with intergenerational variation in environmental selection, yielding alternative phenotypes better suited for the environment in which they occur. Here we use mycalesine butterflies, which express distinct seasonal forms in response to wet-dry seasonal environments, to explore whether seasonal polyphenism extends to secondary sexual traits. Sex pheromones, which are produced by androconial patches on the wings of males, are a key determinant of mating success in these species. Through a series of field sampling, reaction norm experiments, pheromone titre quantification, and mate competition experiments, this study reveals that the size of the androconial patch on the forewing is mediated by the temperatures experienced during development, which correspond to the ecological conditions during the alternative wet and dry seasons in the wild. Furthermore, in one of the species, Bicyclus anynana, larger forewing patches are associated with both an increase in the production of pheromone components as well as the likelihood of mating. Taken together, these findings indicate that plasticity in androconial patches may be an adaptation to seasonal fluctuations in the environment as it favours reproductive success in the conditions in which each seasonal form flies. We discuss our findings in the context of seasonal differences in the optimal tradeoff between reproduction and survival.