Ecological and genetic distinctiveness of socially hybridogenetic lineages of Pogonomyrmex harvester ants at regional and local scales

Interspecific hybridization generates novel combinations of alleles, whose persistence depends on the extent to which hybrids are reproductively isolated and ecologically competitive in the environments in which they occur. In the ant genus Pogonomyrmex, two historical hybrid zones between the congeners P. rugosus and P. barbatus have given rise to socially hybridogenetic populations, in which two co-occurring lineages derived from the two species obligately interbreed to produce F1 hybrid workers, but only within-lineage crosses develop into reproductive females. We tested whether two independently-derived hybridogenetic populations (J1/J2 and FGH1/FGH2) occupy distinct ecological niches at a regional scale, and whether their occupancy patterns are consistent with hybrid superiority in intermediate or novel habitats. We then investigated ecological habitat segregation and reproductive isolation at the local scale where hybridogenetic and parental colonies overlap. Niche modeling revealed significant differences between the two parental species, with P. rugosus occurring in drier and more seasonal habitats than P. barbatus. Both hybridogenetic taxa occupied distinct niches from the two parents and from one another. The FGH1/FGH2 population showed high niche overlap with both parents, consistent with displacement the parental species in intermediate areas. In contrast, J1/J2 occupied a unique habitat most similar to P. rugosus, but with higher and more concentrated winter precipitation. There was virtually no interbreeding at contact sites between a parent species and the hybridogenetic lineage pair. Ecologically, both adult colonies and founding queens were spatially segregated at five of the six sites, with colony identity significantly predicted by microhabitat characteristics associated with moisture and resource availability. Altogether, these results suggest that the socially hybridogenetic lineages have become evolutionarily independent from their parent species, with both bounded hybrid superiority and ecological novelty serving as drivers of the ecological persistence of these unusual two-lineage interdependent systems.