Genetic caste determination in dependent lineages of Pogonomyrmex barbatus and Pogonomyrmex rugosus

A central trait of highly-social insects is reproductive division of labor in which the environment determines caste (queen or worker) of immature individuals. However, colonies from many populations of Pogonomyrmex exhibit genetic caste determination (GCD) generated by the interbreeding of two reproductively isolated yet interdependent lineages. GCD relies on obligate polyandry, as queens must mate with a same-lineage male to generate reproductive queens and an alternate-lineage male to generate workers. We label these dependent lineage (DL) systems, because both lineages must be sustained in the population to generate functional GCD colonies. Despite these constraints, a geographical survey revealed the GCD phenotype as widespread occurring in 20 of 46 sampled populations. Mapping the GCD phenotype onto a mtDNA phylogeny indicates that dependent lineages of P. rugosus were derived following the origin of GCD in P. barbatus . We speculate that the origin of GCD involved a nuclear mutation resulting in genetic conflict that first separated, then maintained allele (or gene set) combinations that confer differences in caste development.; DL systems seem to prosper despite the costs associated with GCD. Queens of GCD colonies produce fewer offspring, and fewer brood with advanced development, as compared to colonies with environmental caste determination. Assuming random mating and the expectation that females mate with three males on average, our results indicate that GCD queens acquiring a high proportion of same-lineage sperm have no fitness. In DL populations with highly skewed lineage frequencies, the costs associated with GCD are borne primarily by the common lineage, indicating that negative frequency dependent selection on colony founding acts to stabilize a DL system. By dissection and microscopy, we determined that queens do not mate within the nest prior to the mating flight. In line with predictions based on initial lineage frequencies, the sex ratio also differed significantly between lineages. When a lineage becomes very rare it produces progressively fewer colonies capable of gyne production suggesting that population sex ratios are an important factor in rare lineage recovery and may establish a deterministic set point from which the frequency of the rare lineage cannot recover.