Laboratory social environment biases mating outcome: a first quantitative synthesis in a butterfly

Abstract

Sexual selection is by essence social selection: an individual’s fitness is partly determined by the phenotype of its social partners (i.e., the social environment). Nevertheless, most behavioral studies on mating patterns and sexual selection are conducted in laboratory standardized conditions, and it is unclear how potential laboratory-induced social biases affect mating outcome. The social environment may actually dictate which of female mate choice or male-male competition is the primary determinant of mating outcome. This matters because we expect sexually selected traits to evolve differently if mating outcome is determined by female mate choice or by male-male competition. We address this issue by performing an in-depth quantitative synthesis testing the effects of common extrinsic (population density, sex ratio), intrinsic (age), and laboratory-induced (cage volume, experimental duration) biases of the social environment of adults on mating outcome. For this, we used the butterfly Bicyclus anynana, as it provides a reasonable sampling of mating experiments in diverse laboratory conditions (i.e., 31 publications from 7 different laboratories since 2001). We found that all tested social environmental variables displayed strong variation across B. anynana mating studies, and that most variables had significant effects usually in interaction with another variable and with opposite effects between sexes. Hence, mating outcome is affected by laboratory biases on the social environment. Our quantitative synthesis offers a first case example of the effects of a pervasive and recurrent issue in animal behavioral research on sexual selection, i.e., the need to root mating experiments in ecologically relevant laboratory environments, in order to produce meaningful results about the selective force(s) driving the evolution of sexually selected traits in nature. Mating outcome is biased by the laboratory social environment in which experiments are conducted. Male and female age, density, ratio, as well as cage volume and experimental duration all affect mating proportions, and this blurs our understanding of how sexual selection shapes sexually selected traits in the wild. This first systematic review was conducted on 31 studies in a single butterfly species, but our results are likely relevant in any taxonomic group.