The mechanisms of socially induced infertility of the highveld mole-rat (Cryptomys hottentotus pretoriae)

Abstract

This thesis explores the intricate mechanisms underlying reproductive suppression and queen succession in the highveld mole-rat (Cryptomys hottentotus pretoriae), a cooperatively breeding social rodent within the family Bathyergidae. In these colonies, a dominant breeding female (the queen) exclusively monopolises reproduction, while subordinate members of both sexes are hysiologically suppressed through a complex interplay of social, hormonal, and ecological factors. Central to this hierarchy and suppression is prolactin (PRL), a key hormone in mammalian reproduction that regulates energy allocation and social behaviours, enforcing infertility among non breeding females (NBFs) and ensuring colony stability. Field and laboratory experiments revealed that PRL levels are modulated by ecological and seasonal influences. During the dry season, elevated PRL levels maintain reproductive suppression, possibly through restricted feeding of subordinates by dominant breeders. In contrast, the wet season, marked by increased food availability, triggers a reduction in PRL levels, enabling partial reproductive activation in NBFs and facilitating dispersal opportunities. Experiments involving forced dispersal and sucrose supplementation demonstrated a direct link between decreased PRL levels, improved energy balance, and reproductive activation. However, the dopamine agonist bromocriptine, typically effective in lowering PRL, failed to do so in highveld mole-rats, suggesting an evolutionary resistance to dopaminergic regulation in the dopamine-prolactin (DA-PRL) axis. The findings underscore the centrality of PRL in maintaining socially induced infertility, shaped by energy dynamics and environmental conditions. This strategy is critical for reproductive suppression in cooperative breeders, balancing ecological pressures, genetic risks, and social stability. Among highveld mole-rats, PRL mediated suppression not only sustains the reproductive hierarchy, but also facilitates colony cohesion. Within intact colonies, PRL levels varied significantly among NBFs, with heavier females—potential "beta queens"—exhibiting lower PRL levels and partial reproductive activation. Upon queen removal, females with the lowest PRL levels were most likely to succeed to new queen status (regardless of their relatedness to the breeding male), supported by elevated testosterone levels that enabled the aggression necessary to dominate rivals. Once the new queen was established, her testosterone levels subsided, reducing prolonged aggression, and stabilising the colony. This chapter also found a minimal influence of genetic relatedness on queen succession, emphasising hormonal regulation over incest avoidance. Yet, despite their tolerance for inbreeding, highveld mole-rats showed a preference for unrelated males when available, highlighting a secondary role for genetic diversity in mate selection. The thesis demonstrates how PRL-mediated physiological suppression underpins reproductive hierarchies, illustrating the delicate balance between ecological, hormonal, and social factors that shape reproductive strategies in inbreeding-tolerant species. In conclusion, this work provides valuable insights into the evolutionary adaptations and hormonal mechanisms that maintain reproductive hierarchies in cooperative breeders. The findings have significant implications for understanding how environmental and social factors influence reproductive dynamics, contributing to a broader knowledge of behavioural ecology and the evolution of sociality in mammals.