Evolutionary history of inquiline social parasitism in Plagiolepis ants

Social parasitism, i.e. the parasitic dependence of a social species on another free-living social species, is one of the most intriguing phenomena in social insects. It has evolved to various levels, the most extreme form being inquiline social parasites which have lost the worker caste, and produce only male and female sexual offspring that are reared by the host worker force. The inquiline syndrome has been reported in 4 species within the ant genus Plagiolepis, in Europe. Whether inquiline social parasitism evolved once or multiple times within the genus remains however unknown. To address this question, we generated data for 5 inquiline social parasites - 3 species previously described and 2 unidentified species - and their free-living hosts from Europe, and we inferred their phylogenetic relationships. We tested Emery's rule, which predicts that inquiline social parasites and their hosts are close relatives. Our results show that inquiline parasitism evolved independently at least 5 times in the genus. Furthermore, we found that all inquilines were associated with one of the descendants of their most related free-living species, suggesting sympatric speciation is the main process leading to the emergence of the parasitic species, consistent with the stricter version of Emery's rule.