Female density-dependent chemical warfare underlies fitness effects of group sex ratio in flour beetles

Abstract

In animals, skewed sex ratios can affect individual fitness via sexual (e.g., intersexual conflict or intrasexual mate competition) or nonsexual (e.g., sex-specific resource competition) interactions. Because most analyses of sex ratio focus on sexual interactions, the relative importance of sexual versus nonsexual mechanisms remains unclear. We tested both mechanisms in the flour beetle Tribolium castaneum, where male-biased sex ratios increase female fitness relative to unbiased or female-biased groups. Although flour beetles show both sexual and nonsexual (resource) competition, we found that sexual interactions did not explain female fitness. Instead, female fecundity was dramatically reduced even after a brief exposure to flour conditioned by other females. Earlier studies suggested that secreted toxins might mediate density-dependent population growth in flour beetles. We identified ethyl benzoquinone and methyl benzoquinone (quinones) as components of adult stink glands that regulate female fecundity. In female-biased groups (i.e., at high female density), females upregulated quinones and suppressed each other’s reproduction. In male-biased groups, low female density and associated low quinone levels maximized fecundity. Thus, females appear to use quinones as weapons for female-specific, density-dependent interference competition. Our results underscore the importance of nonsexual interference competition that may often underlie the fitness consequences of skewed sex ratios.