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. However, while 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, while 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.

Methods
By adopting a powerful approach to studying adaptation -experimental evolution- we investigate, for the first time, the independent and interactive effects of sexual selection and selection associated with metapopulation structure on the evolution of movement activity. As a model system, we used the seed beetle Callosobruchus maculatus, a polygamous species characterized by intense sexual selection and sexual conflict. Beetles from a same original population were cultured in a 2x2 cross-classified selection experiment, whereby binary selection treatments associated with the intensity of sexual selection (high, under a polygamous mating system, or minimal, under an enforced monogamous mating system), and associated with metapopulation structure (yes/no), were crossed. Each of the resulting four combinations of selection treatments was replicated across four populations (Rodriguez-Exposito et al. 2021 for further details), over 79 generations. Subsequently, after a generation of common garden breeding, we measured the movement activity of individuals subjected to the four selection regimes (each combination of selection treatments) under two different environmental contexts (with and without cues from conspecifics; henceforth competitive and non-competitive environment, respectively).

See methods section of the associated paper for details on the experimental protocol and data processing for analysis.