Cooperation with non-kin: Context-dependent acceptance of alien queens by polygynous ant workers

Relatedness underlies the evolution of reproductive altruism, yet eusocial insect colonies occasionally accept unrelated reproductive queens. To better understand this seemingly paradox, we investigated whether acceptance of unrelated queens by workers is an incidental phenomenon resulting from failure to recognize non-nestmate queens, or whether it is an adaptive behavior favored in specific contexts where cooperation is preferable to rejection. Our study system is the socially polymorphic Alpine silver ant, Formica selysi. Within populations some colonies have a single queen (monogynous), and others have multiple, sometimes unrelated, breeding queens (polygynous). Social organization is determined by a supergene with two haplotypes. In a first experiment we investigated whether workers from polygynous colonies were inherently more prone to accepting unrelated queens than workers from the alternate, monogynous social form. We found that workers rejected all alien queens, independently of their social origin and of the number of queens heading their colony. We then investigated whether queen acceptance was favored in specific conditions. We found that workers from polygynous colonies accepted alien queens when these queens were accompanied by workers. These results show that workers flexibly adjust their acceptance of alien queens according to the situation. We discuss how conditional acceptance of unrelated queens may be adaptive by providing benefits through increased colony size and/or genetic diversity, and by avoiding the rejection costs resulting from fighting.

Sociogenetic Organization of the Red Honey Ant (Melophorus bagoti)

Kin selection and inclusive fitness are thought to be key factors explaining the reproductive altruism displayed by workers in eusocial insect species. However, when a colony’s queen has mated with <2 males, workers may increase their fitness by producing their own male offspring. Conversely, when the queen has mated with ≥2 males, workers are expected to increase their inclusive fitness by eschewing the production of their sons and preventing other workers from reproducing as well. Here, we investigated sociogenetic structure and worker reproduction in the red honey ant, Melophorus bagoti. Morphometric analyses revealed that workers belong to one of two distinct subcastes: they are either majors or minors. Using DNA microsatellite markers, we showed that all the colonies had a single, multiple-mated queen and that there was no relationship between worker patriline and worker subcaste. Furthermore, we found that workers were producing males in the presence of the queen, which contrasts with the predictions of inclusive fitness theory. Although our results are based on a small sample, they can serve as the foundation for future research examining worker reproduction in M. bagoti.

A split sex ratio in solitary and social nests of a facultatively social bee

A classic prediction of kin selection theory is that a mixed population of social and solitary nests of haplodiploid insects should exhibit a split sex ratio among offspring: female biased in social nests, male biased in solitary nests. Here, we provide the first evidence of a solitary–social split sex ratio, using the sweat bee Megalopta genalis (Halictidae). Data from 2502 offspring collected from naturally occurring nests across 6 years spanning the range of the M. genalis reproductive season show that despite significant yearly and seasonal variation, the offspring sex ratio of social nests is consistently more female biased than in solitary nests. This suggests that split sex ratios may facilitate the evolutionary origins of cooperation based on reproductive altruism via kin selection.

Social enforcement depending on the stage of colony growth in an ant

Altruism is a paradox in Darwinian evolution. Policing is an important mechanism of the evolution and maintenance of altruism. A recently developed dynamic game model incorporating colony demography and inclusive fitness predicts that, in hymenopteran social insects, policing behaviour enforcing reproductive altruism in group members depends strongly on the colony growth stage, with strong policing as the colony develops and a relaxation of policing during the reproductive phase. Here, we report clear evidence supporting this prediction. In the ant Diacamma sp., reproduction by workers was suppressed by worker policing when the colony was small, whereas in large, mature colonies worker policing was relaxed and worker-produced males emerged. Conditional expression of traits can provide strong empirical evidence for natural selection theory if the expression pattern is precisely predicted by the theory, and our results illustrate the importance of intracolony population dynamics in the evolution of social systems.

Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister–sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that ‘family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism’.

Environmentally induced responses co-opted for reproductive altruism

Reproductive altruism is an extreme form of altruism best typified by sterile castes in social insects and somatic cells in multicellular organisms. Although reproductive altruism is central to the evolution of multicellularity and eusociality, the mechanistic basis for the evolution of this behaviour is yet to be deciphered. Here, we report that the gene responsible for the permanent suppression of reproduction in the somatic cells of the multicellular green alga, Volvox carteri , evolved from a gene that in its unicellular relative, Chlamydomonas reinhardtii , is part of the general acclimation response to various environmental stress factors, which includes the temporary suppression of reproduction. Furthermore, we propose a model for the evolution of soma, in which by simulating the acclimation signal (i.e. a change in cellular redox status) in a developmental rather than environmental context, responses beneficial to a unicellular individual can be co-opted into an altruistic behaviour at the group level. The co-option of environmentally induced responses for reproductive altruism can contribute to the stability of this behaviour, as the loss of such responses would be costly for the individual. This hypothesis also predicts that temporally varying environments, which will select for more efficient acclimation responses, are likely to be more conducive to the evolution of reproductive altruism.