Evolutionary association between subterranean lifestyle and female sociality in rodents

Subterranean rodents are a good model system to examine adaptive evolution of social organization. Life underground has been proposed either to favor solitariness or, to the contrary, to promote sociality. In concordance with the first idea, most specialized diggers are solitary. However, group-living in several unrelated subterranean rodent species and especially eusociality in two genera of African mole-rats, the Bathyergidae, seem to support the second hypothesis. Thus, none of the two models is fully consistent with empirical data. Here we apply the comparative phylogenetic method to test an evolutionary correlation between fossoriality and female social strategy (solitary breeding vs breeding in group). Both characters show very strong phylogenetic signal, and we found a significant correlation between them. Subterranean lifestyle is readily acquired under female sociality. By contrast, the transition to life underground is extremely unlikely under female solitariness. Thus, not only social behavior may be affected by ecological specialization as it is widely assumed, but it can itself restrain the range of possible specializations. The rates of transition from sociality to solitariness are equal under subterranean and surface-dwelling lifestyle. Sociality loss is irreversible in subterranean lineages, unlike surface-dwelling lineages. Based on the revealed transition rates we suggest that all lineages of subterranean rodents have gone through the stage of cooperation at the beginning of their evolutionary track, whereas group-living is selected against in highly specialized diggers. An odd pattern of distribution of sociality across and within truly subterranean taxa probably derives from the influence of extrinsic factors in combination with phylogenetic inertia.