Reconstructing the relatedness of cooperatively breeding queens in the Panamanian leaf-cutting ant Acromyrmex echinatior (Hymenoptera: Formicidae)

The evolution of permanent inquiline social parasites in ants has been conjectured to be facilitated by secondary polygyny, that is, the re-adoption of new queens into existing mature colonies. This idea was first formulated by Wasmann, Wheeler, and Emery more than a century ago. Emery predicted that inquilines should be the sister-lineages of their hosts, which prompted Alfred Buschinger to propose that they evolve by sympatric speciation. However, these scenarios hinge on two vital conditions that have not been quantitatively documented: 1. That host sister species are secondarily polygynous and primarily recruit close kin, and 2. That such adoptions are prone to occasional mistakes that would select for the condition-dependent expression of exploitative traits and reproductive isolation by disruptive selection. Here, we use a long-term data set on the leaf-cutting ant Acromyrmex echinatior (FOREL, 1899), known to have a closely related inquiline social parasite A. insinuator SCHULTZ, BEKKEVOLD & BOOMSMA, 1998, to address the first of these conditions. We estimate the frequency of secondary polygyny and the degree to which cooperatively breeding queens are related. We find that the overall frequency of polygynous colonies is ca. 8% and that polygynous colonies typically have two queens. Most queen pairs are first-degree relatives, consistent with colonies adopting one or two daughters either before or just after becoming orphaned. However, we also document a few pairs of cooperatively breeding queens that are unrelated and estimate that this social structure may apply to ca. 20% of the polygynous colonies, and thus ca. 1% of all colonies. Our findings show that the breeding system of A. echinatior matches the polygyny characteristics that are believed to facilitate the emergence of socially parasitic queen morphs.