Context-dependent vaginal perforation in subordinate female naked mole-rats (Heterocephalus glaber): insights into reproductive plasticity and social modulation

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Abstract While reproductive skew occurs in many social species, it is particularly pronounced in eusocial systems, where reproduction is restricted to a single breeding pair or a few individuals. In naked mole-rats ( Heterocephalus glaber ), this skew is particularly high, with reproduction typically monopolized by a single dominant female, while all other females remain non-reproductive. However, some subordinate females exhibit signs of reproductive activation, such as vaginal perforation, despite the presence of a breeding queen. This study examined long-term (e.g. birth mass, litter order, growth rate) and short-term (e.g. social context, queen status) predictors of vaginal perforation in subordinate females from eight captive colonies. Overall, 41.2% of adult subordinate females displayed vaginal perforation. The presence of an active, dominant queen did not significantly reduce the probability of subordinate perforation. Instead, dynamic maternal and colony-level factors such as queen pregnancy stage and colony sex ratio, as well as individual-level characteristics including litter identity, body mass and relatedness to the queen emerged as significant predictors. Perforation events frequently coincided with the queen’s late pregnancy and with periods of social instability. The probability of perforation in subordinate females did not differ significantly between established and newly established colonies. These findings suggest that vaginal perforation may represent a reversible physiological state reflecting partial reproductive activation in response to specific social or reproductive cues. This interpretation aligns with the “peace incentives” hypothesis, which proposes that dominant individuals may tolerate limited subordinate activation to reduce conflict. This study provides evidence for socially and physiologically modulated variation in reproductive phenotype among subordinate females in a vertebrate eusocial system.

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