Population genomics of the inquiline social parasite Acromyrmex insinuator and its leaf-cutting ant hosts A. echinatior and A. octospinosus reveals cryptic differentiation and reduced efficiency of selection in the parasite

Inquiline social parasites usurp colonies of closely related host ants to exploit their social resources. They are almost invariably rare, patchily distributed and difficult to study. Building on almost 25 years of fieldwork in Panama on the social parasite Acromyrmex insinuator and its hosts A. echinatior and A. octospinosus , we use population genomic analyses to test three hypotheses about the evolution of inquiline social parasites: (1) that parasites have extremely reduced effective population sizes, (2) that their genetic variation at coding and non-coding sites shows signatures of eroded adaptive potential, and (3) that they are fully reproductively isolated from their sympatric hosts. We show that the two host species are completely distinct, whereas the parasite has dramatically reduced genetic diversity and effective population size, despite minor ongoing gene flow with its primary host A. echinatior . Non-synonymous sites evolve at rates nearly indistinguishable from synonymous sites, indicating a marked reduction in the efficiency of natural selection, consistent with the short evolutionary lifespan of inquiline social parasite lineages. Finally, we uncover clear sub-structure in the A. insinuator population, with two genetically distinct lineages co-occurring in the Panama Canal Zone that significantly differ in their likelihood of exploiting the secondary host A. octospinosus .