Experimental evolution reveals differential evolutionary trajectories in male and female activity levels in response to sexual selection and metapopulation structure.

Behavior is central to interactions with the environment and thus has significant consequences for individual fitness. Sexual selection and demographic processes have been shown to independently shape behavioral evolution. Although some studies have tested the simultaneous effects of these forces, no studies have investigated their interplay in behavioral evolution. We applied experimental evolution in the seed beetle Callosobruchus maculatus to investigate, for the first time, the interactive effects of sexual selection intensity (high [polygamy] vs. minimal [enforced monogamy]) and metapopulation structure (yes/no) on the evolution of movement activity, a crucial behavior involved in multiples functions (e.g., dispersal, predator avoidance, or resource acquisition) and thus, closely related to fitness. We found that the interactive effects of the selection regimes did not affect individual activity, which was assayed under two different environments (absence vs. presence of conspecific cues from both sexes). However, contrasting selection regimes led to sex- and context-dependent divergence in activity. The relaxation of sexual selection favored an increase in female, but not male, movement activity that was consistent between environmental contexts. In contrast, selection associated with the presence/absence of metapopulation structure led to context-dependent responses only in male activity. In environments containing cues from conspecifics, males from selection lines under population subdivision showed increased levels of activity compared to those assayed in an environment devoid of conspecifics cues, whereas the opposite was true for males from panmictic lines. These results underscore that both the effects of sexual selection and population spatial structure may be crucial in shaping sex-specific behavioral evolution.