Resolution of Reproductive Conflict in Naked Mole Rats: Stress Response and the Evolutionary Consequence

Naked mole rat (NMR) is one of the only two mammal species with eusociality, in which system reproduction is extremely restricted to the queen and one to three breeding males, while other members cooperate to defend the colony and care for the pups. This unusual social structure might give rise to reproductive conflict between sexes and casters, since all members in fact have reproductive potential. To elucidate how NMRs regulate this conflict, we compared both the transcriptomes and methylomes for the brain and gonadal tissues between breeders and non-breeders. By performing functional analysis and network analysis, we discovered that stress response system, particularly genes encoding NPY and CRH, may inhibit the hypothalamic–pituitary–gonadal (HPG) axis in non-breeders by regulating GnRH and LH. Besides, the downstream process of HPG axis - estrogen synthesis pathway - is destructed in the ovaries of non-breeding females, indicating a lack of estrogen synthesis in subordinate females.  This, in turn, may feed back to the brain and regulate the reproductive and behavioral difference, which explains the reproductive behavior difference between castes. Furthermore, to understand the evolutionary consequence of the reduced reproductive conflict, we scanned for the pseudo-genes and analyzed the evolution rate of male bias genes. In contrast to other close-related non-social rodents, pseudo-genes in NMRs are significantly enriched in spermatogenesis related functions, and male-bias genes evolve faster than non-bias genes, suggesting a reduced sperm competition due to the special reproductive conflict resolving system. Therefore, NMRs resolve reproductive conflict by regulating the HPG axis via the stress response system, and this further lead to a relaxed selection in male-bias genes.