Shift in frequency-dependent selection across the life-cycle in obligately interbreeding harvester ant lineages

Abstract

The long-term persistence of hybridogenetic systems, in which one genetic lineage is dependent on another as a sperm host, is paradoxical because they require continual coexistence between ecological competitors. Several species of ants display a social form of hybridogenesis, in which two distinct genetic lineages obligately interbreed to produce sterile workers, while intra-lineage progeny become the reproductives. A recent model suggests that persistence of such a system depends on the relative strengths of negative frequency-dependent selection acting during colony growth and positive frequency-dependent selection during reproduction. We used path analysis to investigate the effect of lineage frequency on reproductive output and colony sex ratio over a single reproductive season in a natural population of the H1/H2 lineage pair in the genus Pogonomyrmex. Results suggest that lineage frequency does impact reproduction via two opposing routes: the more common lineage procures more same-lineage mates, resulting in a higher proportion of same-lineage mates increases reproduction through higher queen-egg availability, but the rarer lineage procures more alternate-lineage mates, yielding a more genetically diverse worker caste that increases productivity. As a result, lineage frequency has only a weakly positive overall effect on colony reproduction, and overall frequency-dependence in this system across the entire life cycle is likely to be negative as predicted by the persistence model.