Developmental divergence: neglected variable in understanding the evolution of reproductive skew in social animals

Unequal reproduction is widespread in animal societies. Over the last decade, there have been several attempts to derive a conceptual framework that allows diverse taxa of invertebrates and vertebrates to be compared with the aim of identifying common causes underlying reproductive division of labor. Sherman et al. (1995) used reproductive skew values, derived from variation in lifetime reproductive success, to classify taxa. Crespi and Yanega (1995), on the other hand, focused on the loss of "totipotency"-the potential throughout a lifetime to exhibit the full behavioral repertoire of the species-and argued that comparisons can only be made between taxa with and without totipotency among group members. Here we argue that the effect of irreversible morphological differences on the variation in lifetime reproductive success of breeders and helpers has been neglected. Such phenotypic specialization originates during development and is not equivalent to behavioral differentiation among adults. We classify social animals into 3 developmental pathways to examine the ontogenetic stage at which irreversible morphological differences arise. This allows for heuristic comparisons of reproductive skew across taxa; it is more useful to compare skew in termites and bees without morphologically specialized breeders and helpers to cooperative breeding birds and mammals than it is to compare them with other insects with morphological castes. Once physical castes have evolved, natural selection will lead to further morphological specialization for increased efficiency at both helping and breeding (e.g., physogastry in insect queens and complete sterility of some social insect workers). Importantly, extreme reproductive skew can be achieved with and without morphologically specialized helpers and breeders, indicating that grouping societies based on their reproductive skew value alone is not useful.