Genomic architecture and evolutionary dynamics of a social niche polymorphism in the California harvester ant, Pogonomyrmex californicus

The societies of social insects are highly variable, including variation in the number of reproductives in a colony. In the California harvester ant, Pogonomyrmex californicus (Buckley 1867), colonies are commonly founded by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), two or more queens cooperate in colony founding (pleometrosis) and continue to share a nest over several years (primary polygyny). Here, we use population genomics and linkage mapping to study the evolutionary dynamics and genetic architecture of this social niche polymorphism.

Our analyses show that both populations underwent consecutive bottlenecks over the last 100,000 generations, particularly decreasing population size in the P-population and that the two populations diverged until 1,000 generations ago, after which gene flow increased again and we found signs of recent genetic admixture between the two populations. We further uncover an 8 Mb non-recombining region segregating with the observed social niche polymorphism, showing characteristics of a supergene comparable to the ones underlying social niche polymorphism in other ant species.

In addition, 57 genes in five genomic regions outside the supergene show signatures of a selective sweep in the P-population, some of which are differentially expressed between haplo- and pleometrotic queens during colony founding. Our findings expose the social niche polymorphism in P. californicus as a polygenic trait involving a supergene.