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. Here we build on almost 25 years of Panamanian fieldwork on the social parasite Acromyrmex insinuator and its A. echinatior and A. octospinosus hosts, to perform a population genomic analysis to test hypotheses that have been suggested to shape the evolution of inquiline social parasites: 1. Do these parasites indeed have extremely reduced effective population size? 2. Does extant genetic variation at coding and non-coding sites carry signatures of erosion of adaptive potential? 3. Has A. insinuator become fully reproductively isolated from its sympatric hosts and how closely related are its primary and secondary host? We show that the two host species are completely distinct and that genetic diversity and effective population size of the social parasite are dramatically reduced despite ongoing but very minor recent gene flow between the parasite and its primary host A. echinatior. We also demonstrate that non-synonymous codon-sites evolved at rates nearly indistinguishable from synonymous codon-sites. This indicates a significant reduction in the efficiency of natural selection consistent with inquiline social parasite lineages generally being evolutionarily short-lived. We finally uncover clear sub-structure in the parasite population, with two genetically distinct lineages occurring in sympatry in the Panama Canal Zone, and with significant differences in their likelihood of exploiting the secondary host A. octospinosus and the primary host from which they segregated sympatrically ca. 1 MYA.