Epigenetic Changes Associated With a Phenotypic Transition in Namibian Cheetahs

In populations with low genetic diversity, the capacity to adapt to environmental change is limited. While epigenetic mechanisms can generate phenotypic plasticity, their role in mediating adaptive life-history transitions in the wild is largely unknown. Here, we show that in adult Namibian cheetahs (Acinonyx jubatus jubatus), a species with remarkably low genetic diversity, the transition from a floater to a male holding a territory is associated with widespread DNA methylation changes, with a predominance of hypermethylation in territorial males. Using paired blood samples collected from the same individuals before and after becoming territorial, we identified differentially methylated genes which function in pathways related to anatomical and head development, brain development and neurodevelopment, cAMP biosynthesis and ion channel transport, consistent with the observed phenotypic shifts in morphology, spatial movement and aggressive behaviour. These findings suggest that DNA methylation mediates this life-history transition at the molecular level. More broadly, they provide rare evidence that epigenetic regulation is relevant in phenotypic diversity within species with low genetic diversity, potentially supporting adaptive potential at the population level.