Unequal reproduction early in a social transition: insights from invasive wasps

Cooperative societies provide mutual benefits that are susceptible to exploitation. In eusocial insects, nestmate queens can differ in their reproductive output, causing asymmetries in the distribution of mutual benefits. Previous studies investigated unequal reproduction in species with a long evolutionary history of cooperative breeding. Here, we leverage a recent transition from predominantly single-queen (monogyne) to multiple-queen (polygyne) colonies in an invasive yellowjacket to investigate whether queens in incipiently polygyne colonies invest equally in reproductive effort or vary in their relative investment in each caste. We excavated nine polygyne Vespula pensylvanica colonies from Hawaii and used restriction site associated DNA sequencing to infer the parentage of worker, male, and gyne (daughter queen) pupae from each nest comb. In four colonies with at least eight gyne pupae, a single queen produced most or all gynes. These queens had no male offspring and few worker offspring, suggesting that a subset of nestmate queens might exploit the collective benefits of newly polygyne societies. In contrast to most queens, gyne-producers had offspring distributed non-randomly across nest combs. Nestmate queens generally exhibited low relatedness levels, which may cause intra-colony conflicts leading to the observed reproductive asymmetries. Overall, these incipiently polygyne colonies are composed of unrelated queens that may be engaged in subtle reproductive conflicts early in an evolutionary transition to polygyny. Our results suggest that rapid, ecologically driven transitions to polygyny among unrelated queens may, at their onset, be vulnerable to reproductive asymmetries that are likely evolutionarily unstable, prone to collapse or strong selection for conflict-reducing mechanisms like policing. Such findings contribute to our understanding of eusocial evolution by uncovering how polygyne queens partition reproduction within the nest in a social wasp.