Peaceful Queen Succession in the Naked Mole Rat

The eusocial naked mole rat exhibits an extreme reproductive skew involving a single queen that monopolizes breeding through behavioral dominance. When reproductive suppression of subordinates is lifted due to removal or death of the queen, subordinate females compete to assume the reproductive role, resulting in intense aggression and intracolony wars. This aggressive reproductive strategy is thought to confer several advantages under stable environmental conditions. However, reliance on a single reproductive female has the potential to create vulnerabilities when challenged with stressors or unstable environments. Thus, in some contexts, non-violent reproductive flexibility may be beneficial. Here, we report a longitudinal study of a captive naked mole rat colony identifying an alternative, mechanistically distinct mode of queen succession in response to external stressors that impair queen reproduction without social disturbance. Elevated colony density was sufficient to impair pup survival but did not alleviate reproductive suppression or trigger aggression in the colony. By contrast, relocating the colony to a new facility caused a long-term pause in the queen’s reproduction, leading to the sequential emergence of her daughters as additional breeders in the absence of fighting or aggression. This resulted in a transient period of peaceful plural breeding with one daughter and ultimately resulted in another daughter assuming the primary reproductive role for the colony. Together our findings support a model in which reproductive ascension is permissive and socially tolerated when the reigning queen’s reproductive function is impaired, thereby expanding the mechanistic framework of naked mole rat eusociality to include peaceful, fertility-based pathways of queen succession.