A solution to a sex ratio puzzle in Melittobia wasps

Abstract

Significance Many social interactions generate a tragedy of the commons, where individuals would do better if everyone cooperated, but selfish interests can select against cooperation. Examples range from the production of extracellular enzymes by bacteria, to cooperative breeding in animals, to female-biased sex ratios in structured populations, where brothers compete for mates. We examined the offspring sex ratios produced by Melittobia wasps in natural populations and found that females adjust their offspring sex ratio in response to both the presence of other females and whether they had dispersed. Dispersal matters because it determines the genetic relatedness between interacting individuals, and so an analogous influence of dispersal would be predicted for a range of cooperative traits, including parasite virulence. The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.