Abstract
Paternal care is rare among mammals and the neural mechanisms governing its emergence are poorly understood(1). We leveraged the natural paternal behaviour of African striped mice (Rhabdomys pumilio)(2,3), and integrated brain-wide cFos mapping, single-nucleus RNA sequencing, virally mediated gene perturbation and environmental manipulation to dissect the neural basis of natural variation in male parenting. Here we find that socio-environmental conditions drive individual variation in male alloparenting such that postweaning social isolation increases paternal care whereas social living in higher density groups increases infanticide. This natural variation in care corresponds to neural activity in the medial preoptic area and changes in correlated activity across brain regions. Within the medial preoptic area, expression of agouti signalling protein (Agouti) in neurons is increased by group housing and is negatively associated with care, and overexpression of Agouti reduces care and enhances infanticide in previously tolerant mice. Naturalistic manipulations further reveal that Agouti integrates long-term housing conditions rather than food availability or hunger. Our findings reveal that variation in male paternal care reflects context-dependent regulation of conserved hypothalamic and melanocortin signalling mechanisms rather than the presence or absence of paternal capacity.