Abstract

Simple SummaryMonogamy is thought to be a major factor having favored the evolution of a non- reproductive worker caste in eusocial insects because it optimizes the relatedness among colony members. However, polyandry evolved secondarily in a large number of species. By increasing the genetic diversity within colonies, multiple mating can enhance worker task efficiency and resistance to diseases. Polyandry may also favor social harmony by reducing worker–queen conflict over male parentage. This is because in colonies headed by a single, multiple-mated queen, workers can increase their inclusive fitness by rearing their brothers (queen sons) rather than their nephews (offspring of other workers). Using DNA microsatellites, we showed that nests of the red honey ant, Melophorus bagoti, are headed by a single, multiple-mated queen. Morphometric analyses revealed two distinct worker subcastes: majors and minors; yet, we found no relationship between worker patriline and worker subcaste. Workers can produce males in the presence of the queen under natural conditions, which contrasts with predictions of inclusive fitness theory.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.

Highlights

  • Reproductive altruism, whereby individuals forgo reproducing themselves to help others produce offspring, has generally been explained by evoking Hamilton’s model of kin selection and inclusive fitness theory [1,2]

  • We found a significant linkage disequilibrium for three pairs of microsatellite loci

  • There was a significant departure from Hardy–Weinberg equilibrium (HWE) for 2 of the 12 microsatellite markers in each population (CAT: Mb06 and Mb24; SPR: Mb21 and Mb28)

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Summary

Introduction

Reproductive altruism, whereby individuals forgo reproducing themselves to help others produce offspring, has generally been explained by evoking Hamilton’s model of kin selection and inclusive fitness theory [1,2]. Relatedness is critical for the evolution of reproductive altruism: it can enhance the helpers’ indirect fitness, since copies of the helpers’ genes are passed on to the subsequent generation by the beneficiary of the altruistic act. Selection will favor altruism if altruists gain more in indirect fitness than they lose by not reproducing. Any infinitesimal benefit of helping one’s parents produce new offspring should favor the evolution of a non-reproductive helper caste. Lifetime monogamy may be evolutionarily sufficient to select for permanently sterile worker castes, such as those seen in eusocial species [3,4,5]

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