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 inP. californicusas a polygenic trait involving a supergene.

Genome assembly and annotation of the California harvester ant Pogonomyrmex californicus

The harvester ant genus Pogonomyrmex is endemic to arid and semiarid habitats and deserts of North and South America. The California harvester ant Pogonomyrmex californicus is the most widely distributed Pogonomyrmex species in North America. Pogonomyrmex californicus colonies are usually monogynous, i.e. a colony has one queen. However, in a few populations in California, primary polygyny evolved, i.e. several queens cooperate in colony founding after their mating flights and continue to coexist in mature colonies. Here, we present a genome assembly and annotation of P. californicus. The size of the assembly is 241 Mb, which is in agreement with the previously estimated genome size. We were able to annotate 17,889 genes in total, including 15,688 protein-coding ones with BUSCO (Benchmarking Universal Single-Copy Orthologs) completeness at a 95% level. The presented P. californicus genome assembly will pave the way for investigations of the genomic underpinnings of social polymorphism in the number of queens, regulation of aggression, and the evolution of adaptations to dry habitats.

High-Quality Genome Assembly and Annotation of the California Harvester Ant Pogonomyrmex californicus (Buckley, 1867)

ABSTRACTThe harvester ant genus Pogonomyrmex is endemic to arid and semiarid habitats and deserts of North and South America and California harvester ant Pogonomyrmex californicus is the most widely distributed Pogonomyrmex species in the North America. P. californicus colonies are usually monogynous, i.e. a colony has one queen. However, in a few populations in California, primary polygyny evolved, i.e. several queens cooperate in colony founding after their mating flights and continue to coexist in mature colonies. Here, we present high quality genome assembly and annotation of P. californicus. The size of the assembly is 241 Mb, which is in good agreement with previously estimated genome size and we were able to annotate 17,889 genes in total, including 15,688 protein-coding ones with BUSCO completeness at the 95% level. This high quality genome will pave the way for investigations of the genomic underpinnings of social polymorphism in queen number, regulation of aggression, and the evolution of adaptations to dry habitats in P. californicus.