No abstract

The ant genus Cardiocondyla is characterized by a bizarre male polymorphism with wingless fighter males and winged disperser males. Winged males have been lost convergently in several clades, and in at least one of them, wingless males have evolved mutual tolerance. To better understand the evolutionary pathways of reproductive tactics, we investigated Cardiocondyla venustula, a species, which in a phylogenetic analysis clusters with species with fighting and species with mutually tolerant, wingless males. Wingless males of C. venustula use their strong mandibles to kill freshly eclosed rival males and also engage in short fights with other adult males, but in addition show a novel behavior hitherto not reported from social insect males: they spread out in the natal nest and defend "territories" against other males. Ant males therefore show a much larger variety of reproductive tactics than previously assumed.

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.

Sex appears to be a rather prosaic and casual event in the life of most social Hymenoptera. In contrast, mating in the ant genus Cardiocondyla is regularly preceded by a prolonged and stereotypic courtship display. Pummeling the head of the female with mandibles and / or antennae and vibrations of the gaster, presumably stridulation, are essential parts of male courtship. The overall structure of the mating pattern is conserved throughout species and between winged and wingless, "ergatoid" males, but exhibits species-specific idiosyncrasies. For example, C. elegans males regularly end the interaction with a female with a short mouth-tomouth contact. Variation in the duration of the precopulatory phase and the copulation itself might reflect different degrees of inter-and intrasexual selection. More information on the dynamics of sperm transfer and the risk and intensity of sperm competition are needed to better understand the evolution of the complex mating behavior in this genus.

Mother-son mating (oedipal mating) is practically non-existent in social Hymenoptera, as queens typically avoid inbreeding, mate only early in life and do not mate again after having begun to lay eggs. In the ant genus Cardiocondyla mating occurs among sib in the natal nests. Sex ratios are extremely female-biased and young queens face the risk of remaining without mating partners. Here, we show that virgin queens of Cardiocondyla argyrotricha produce sons from their own unfertilized eggs and later mate with them to produce female offspring from fertilized eggs. Oedipal mating may allow C. argyrotricha queens to found new colonies when no mating partners are available and thus maintains their unusual life history combining monogyny, mating in the nest, and low male production. Our result indicates that a trait that sporadically occurs in solitary haplodiploid animals may evolve also in social Hymenoptera under appropriate ecological and social conditions.