Female Chemical Warfare Drives Fitness Effects of Group Sex Ratio

Abstract

SUMMARYIn animals, skewed sex ratios can affect individual fitness either via sexual interactions (e.g. intersexual conflict or intrasexual mate competition) or non-sexual interactions (e.g. sex-specific resource competition). Because most analyses of sex ratio focus on sexual interactions, the relative importance of these mechanisms remains unclear. We addressed this problem using 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 non-sexual (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 quinones (secreted toxins) might mediate density-dependent population growth in flour beetles. We identified ethyl- and methyl-benzoquinone (EBQ and MBQ) as the primary 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 lead to low quinone levels, allowing higher fecundity. Thus, quinones serve both as indicators and mediators of female competition, resulting in the observed fitness decline in female-biased groups. Our results underscore the importance of non-sexual interference competition that may often underlie the fitness consequences of skewed sex ratios.