The rarity of multiple mating by females in the social Hymenoptera

Abstract

Interest in how often female social insects mate is particularly intense because of its impact on sociality and because of the well-known extreme multiple mating in honeybees. With multiple mating, worker to brood relatedness decreases but worker versus queen interests often converge. The overwhelming majority of species of social ants, bees, and wasps mate only once. Even those species where some females mate multiply typically have effective mate numbers close to one. Ants have effective mate numbers of 1.43, which drops to 1.15 if the advanced fungus growers (2.14) and harvester ants (6.76) are excluded. Honeybees have effective mate numbers of 12.48. Stingless bees and bumblebees have effective mate numbers of only 1.06 and 1.02 respectively. Polistine wasps have effective mate numbers of 1.01. Vespine wasps have effective mate numbers of 1.12 excluding only Vespula which has effective mate numbers of 3.68. Favoring the very low mate numbers we observe for nearly all female social insects is the narrow time window for mating, lack of material gain from males, lack of male ability to harass females (who must move their sting aside to mate in most species), and lack of paternal care. Single mating may be further favored by the apparent lack of any post-copulatory sperm discrimination mechanisms. Leks and male territories, which are common in social insects, make it easier for females to choose the single best mate, further contributing to low mate numbers. Multiple mating is a rare, derived trait in a generally single-mating group. Single mating may have facilitated the origins of sociality in the Hymenoptera because it confers higher relatedness among potential workers and the brood they care for. The rare exceptions to low mate numbers all come from highly social species with single queens, morphological castes, and many workers. Multiple mating might be stable in highly social species because their highly specialized workers have few selfish responses to lowered relatedness. The unusual cases of multiple mating are most likely to be selected for because they increase genetic diversity in the brood, though empirical support for specific genetic diversity hypotheses has proved to be elusive. What is clear is that single mating is predominant in this large, evolutionarily and ecologically successful group.