Linked supergenes underlie split sex ratio and social organization in an ant

Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent–offspring conflict, genomic conflict, and cooperative breeding. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work predicted that worker control of sex ratio and variation in relatedness asymmetry among colonies would cause each colony to specialize in the production of one sex. While some empirical tests supported theoretical predictions, others deviated from them, leaving many questions about how split sex ratio emerges. One factor yet to be investigated is whether colony sex ratio may be influenced by the genotypes of queens or workers. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens future research on the evolutionary drivers of split sex ratio.

Sibling quality and the haplodiploidy hypothesis

The ‘haplodiploidy hypothesis’ argues that haplodiploid inheritance in bees, wasps, and ants generates relatedness asymmetries that promote the evolution of altruism by females, who are less related to their offspring than to their sisters (‘supersister’ relatedness). However, a consensus holds that relatedness asymmetry can only drive the evolution of eusociality if workers can direct their help preferentially to sisters over brothers, either through sex-ratio biases or a pre-existing ability to discriminate sexes among the brood. We show via a kin selection model that a simple feature of insect biology can promote the origin of workers in haplodiploids without requiring either condition. In insects in which females must found and provision new nests, body quality may have a stronger influence on female fitness than on male fitness. If altruism boosts the quality of all larval siblings, sisters may, therefore, benefit more than brothers from receiving the same amount of help. Accordingly, the benefits of altruism would fall disproportionately on supersisters in haplodiploids. Haplodiploid females should be more prone to altruism than diplodiploid females or males of either ploidy when altruism elevates female fitness especially, and even when altruists are blind to sibling sex.

The benefits of grouping as a main driver of social evolution in a halictine bee

Over the past decade, the cause of sociality has been much debated. Inclusive fitness [brin Hamilton’s rule (br−c> 0)] has been criticized but is still useful in the organization of a framework by elucidating mechanisms through whichbr(benefit × relatedness) becomes larger thanc(cost). The beeLasioglossum baleicumis suitable for investigation of this issue because of the sympatric occurrence of both social and solitary nesting in its populations. We show that a large part (approximately 92%) of the inclusive fitness of a eusocial worker can be attributed to the benefits of grouping. A 1.5-fold relatedness asymmetry benefit in singly mated haplo-diploids explains a small part (approximately 8.5%) of the observed inclusive fitness. Sociality enables this species to conduct foraging and nest defense simultaneously, which is not the case in solitary nests. Our results indicate that this benefit of grouping is the main source of the increased inclusive fitness of eusocial workers.