Gene dynamics of haplodiploidy favor eusociality in the Hymenoptera.

Abstract

The problem of whether haplodiploidy is responsible for the frequent evolution of eusociality in the Hymenoptera remains unresolved. The little‐known “protected invasion hypothesis” posits that because a male will transmit a new allele for alloparental care to all his daughters under haplodiploidy, such an allele has a higher probability of spreading to fixation under haplodiploidy than under diploidy. This mechanism is investigated using the mating system and lifecycles ancestral to eusocial lineages. It is shown that although haplodiploidy increases the probability of fixation of a new allele, the effect is cancelled by a higher probability of the allele arising in a diploid population. However, the same effect of male haploidy results in a 30% lower threshold amount of reproductive help by a worker necessary to favor eusociality if the sex ratio of dispersing first‐brood offspring remains even. This occurs because when first‐brood daughters become workers, the sex ratio of dispersing first‐brood offspring becomes male‐biased, selecting for an overall female‐biased first‐brood sex ratio. Through this mechanism, haplodiploidy may favor eusociality in the absence of a female‐biased sex ratio in dispersing reproductive offspring. The gene‐centric approach used here reveals the critical role of male haploidy in structuring the social group.