Kumi O Kuroda, Kansai Fukumitsu, Takuma Kurachi, Nami Ohmura, Yuko Shiraishi, Chihiro Yoshihara

Mammalian parental care is highly mother-biased, prompting researchers to presume its connection to female reproductive behavior and physiology, not male. However, recent findings in neurobiological studies suggest the opposite. Considering the evolutionary path of mammalian parental care, the ancestral form of vertebrate parental care appears to be male-biased as in living teleosts (bony fish), and originated from egg guarding as an extension of territorial behavior. Phylogenetic analyses suggest that in basal tetrapods, the harsh reproductive environments have facilitated terrestrial adaptation and extensive parental investment in females, and salamander-like basal amniotes exhibited extended egg retention in female bodies. Molecular and fossil evidence indicates that synapsids that have later evolved into mammals have already performed extensive maternal care including egg/offspring hydration in the Carboniferous period. Then the nocturnal adaptation in Jurassic mammaliaforms promoted endothermy and prolonged maternal care for thermal control and lactation. This situation may have added nutritional gate control to the offspring care circuit to balance parental provisioning with maternal homeostatic needs. Combining these paleontological, comparative ecological, and neuromolecular findings, we propose that the mammalian parenting circuit may be derived from MPOA neurons controlling reproductive behaviors during the terrestrial adaptation in anamniotes, either by divergent or parallel evolution. Next, we discuss another long-postulated hypothesis that complex affiliative sociality among adults, including group living, cooperative infant care, empathy, and altruism, may have emerged primarily for extended support of the offspring growth, utilizing the established maternal care circuit in mammals. These evolution-informed working hypotheses may also help dissect the neural basis of the complex cognitive functions in mammals.