Worker Reproduction in the Higher Eusocial Hymenoptera

Worker reproduction (i.e., the parthenogenetic production by workers of males and, more rarely, females) is very widespread in the higher eusocial Hymenoptera (bumble bees, stinglees bees, honey bees, vespine wasps, higher ants). Examples are given in the text. The mutualistic theory ("hopeful reproductive" hypothesis) of hymenopteran eusociality (semisocial route) states that the first workers were reproductive because the possibility of future reproduction was the condition for their originally working. In Hamilton's kinship theory (subsocial route) workers produce males on account of their greater relatedness to sons than to brothers. Several recent models indicate that worker male production could have facilitated the evolution of eusociality. Queen control (queen inhibition of worker fertility) arises because queens are more closely related to their own than to workers' offspring, and explains why present-day workers are most reproductive in queenless conditions. Conversely worker reproduction in queenright colonies (i.e., colonies containing the maternal queen) reflects selection on workers to evade queen control Optimization models predict that workers should produce all or none of a colony's males. Although workers in some species produce 100 per cent of the males, reproductive workers more usually produce an extremely variable proportion of males. When workers reproduce, the expected equilibrium sex ratios change; but the information needed to assess the importance for sex-ratio determination of worker male production is lacking. Kinship theory suggests that polygyny (multiple queens) and multimple mating both promote queeright worker reproduction by reducing intracolony genetic relatedness. The analysis of data assembled on 49 ant species reveals that workers in monogynous species (i.e., with one queen per colony) reproduce moslty in queenless conditions, whereas those in polygynous species reproduce in queenless and queenright conditions equally often, in agreement with kinship theory. Monogyny could favor a reproductive worker caste becuse the high probability of colony orphanage allows workers greater opportunity to reproduce free from queen control. The ability of workers to reproduce has important consequence for colony organization and function. These include (1) the extent and nature of queen control of worker fertility, such control being viewed as the outcome of an "arms race" with workers over male parentage; (2) the occurrence of dominance behavior, egg cannibalism, brood destruction, and possibly even matricide in colonies with reproductive workers; (3) reduced colony efficiency and the system of temporal division of labor based on worker age and ovarian development; and(4) the rarity of physical castes among workers. For all these reasons, worker reproduction is crucial to our understanding of hymenopteran eusociality.