Abstract
Studies on sex ratios in social insects provide among the most compelling evidence for the importance of kin selection in social evolution. The elegant synthesis of Fisher's sex ratio principle and Hamilton's inclusive fitness theory predicts that colony-level sex ratios vary with the colonies' social and genetic structures. Numerous empirical studies in ants, bees, and wasps have corroborated these predictions. However, the evolutionary optimization of sex ratios requires genetic variation, but one fundamental determinant of sex ratios - the propensity of female larvae to develop into young queens or workers ("queen bias") - is thought to be largely controlled by the environment. Evidence for a genetic influence on sex ratio and queen bias is as yet restricted to a few taxa, in particular hybrids.Because of the very short lifetime of their queens, ants of the genus Cardiocondyla are ideal model systems for the study of complete lifetime reproductive success, queen bias, and sex ratios. We found that lifetime sex ratios of the ant Cardiocondyla kagutsuchi have a heritable component. In experimental single-queen colonies, 22 queens from a genetic lineage with a highly female-biased sex ratio produced significantly more female-biased offspring sex ratios than 16 queens from a lineage with a more male-biased sex ratio (median 91.5% vs. 58.5% female sexuals). Sex ratio variation resulted from different likelihood of female larvae developing into sexuals (median 50% vs. 22.6% female sexuals) even when uniformly nursed by workers from another colony.Consistent differences in lifetime sex ratios and queen bias among queens of C. kagutsuchi suggest that heritable, genetic or maternal effects strongly affect caste determination. Such variation might provide the basis for adaptive evolution of queen and worker strategies, though it momentarily constrains the power of workers and queens to optimize caste ratios.
Highlights
Studies of intra- and interspecific variation of sex ratios in the social Hymenoptera provide among the most convincing support for the importance of inclusive fitness in evolution
Workers appear to be capable of biasing sex allocation, i.e., via the selective culling of male larvae or biasing the development of sexuals from female larvae, while in other species a compromise between the interests of queens and workers is achieved (e.g., [7,8,9,10])
By comparing sex ratios among females belonging to different genetic lineages of C. kagutsuchi we studied whether this natural variation might have a heritable basis
Summary
Studies of intra- and interspecific variation of sex ratios in the social Hymenoptera (bees, wasps, and ants) provide among the most convincing support for the importance of inclusive fitness in evolution. Workers appear to be capable of biasing sex allocation, i.e., via the selective culling of male larvae or biasing the development of sexuals from female larvae, while in other species a compromise between the interests of queens and workers is achieved (e.g., [7,8,9,10]). Despite this compelling evidence, one fundamental assumption of sex ratio theory has remained largely untested: the optimization of sex ratios in evolution requires heritable genetic variation in this trait. The importance of genetic variation on queen bias has rarely been documented, with the best evidence coming from hybrid lineages of harvester ants, where caste is exclusively determined by genotype (e.g., [14,15,16,17]), and cross-fostering experiments in the acorn ant Temnothorax curvispinosus [18]
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