Inbreeding preference emerges in female guppies in a socially complex setting

Animals are typically expected to avoid mating with relatives due to the costs associated with incestuous matings. Yet for more than four decades, theoretical models have consistently suggested that animals should tolerate, or even prefer, mating with relatives under a broad range of conditions. However, empirical studies that evaluate inbreeding avoidance under alternative social and sexual contexts remain scarce. Here, we investigate how experimental variation in sexual and social complexity influence precopulatory inbreeding avoidance behaviors in the guppy Poecilia reticulata, a species known to experience inbreeding depression. In an integrated set of experiments, we examined if sexual and affiliative behaviors of virgin and experienced females and males were differentially directed towards either related or unrelated individuals. In simplistic social interactions, neither virgin nor experienced females or males showed a preference for related or unrelated partners. In contrast, we detected sex-specific responses to relatives in the more sexually and socially complex free-swimming arenas. Females exhibited a stronger preference towards related males regardless of mating experience, while male preference remained unchanged. Overall, these findings challenge previous reports of preference shifts between virgin and experienced female guppies and suggest that inbreeding avoidance behaviors may be less prevalent in complex social environments than previously thought.