Phylogenomics of Cervidae provides insights into antler origin and evolution

Antlers are the only fully annually regeneratable organs in mammals. However, the genetic basis underlying their origin and evolution in Cervidae, as well as the significant morphological differences among tribes, remains poorly understood. This study presents six high-quality chromosome-level genomes of cervids spanning four tribes, including the first genome assembly of the tufted deer (Elaphodus cephalophus). Investigation into the Cervidae lineage discover that the formation of antler is explained by positive selection acting on pathways related to stem cell differentiation and bone metabolism, with the implicated genes being highly expressed in the antler developmental and regenerative tissue regions. Tribe-specific positively selected genes in Cervini or Odocoileini further reveal that key signaling pathways, notably the RAS/MAPK pathway, were convergently selected during the origin and enhancement of antlers. Moreover, relaxed selection genes in antler-less Chinese water deer depicts oncogenesis-tumor suppression trade-offs and bone metabolism, suggesting a rewiring of regulatory homeostasis. These findings highlight how antler evolution reshaped physiological trade-offs, including reduced cancer risk and cyclic bone remodeling. This study provides novel insights into the evolution and diversification of antlers and their co-evolved physiological processes, including low cancer incidence and cyclic physiological osteoporosis, while establishing genomic resources for studies on mammalian regeneration.