Early hominin arrival in Southeast Asia triggered the evolution of major human malaria vectors

Abstract Some species of the Leucosphyrus Group of Anopheles mosquitoes in Southeast Asia are highly anthropophilic and efficient vectors of human malaria parasites, while others primarily feed on non-human primates (NHP) and transmit NHP malaria parasites. The evolutionary history of this group, particularly the origin of anthropophily, was studied using phylogenomic analysis of 2,657 high-confidence nuclear single-copy orthologous genes and 13 mitochondrial protein coding genes from 40 individuals of 11 species. Molecular dating and ancestral state reconstruction revealed that monkey-feeding is ancestral with speciation of monkey-feeding species dating to the Pliocene within Sundaland (Malay peninsula, Borneo, Sumatra and Java) which was covered in tropical rain forests during this period. Although less parsimonious alternatives cannot be excluded, molecular dating, ancestral state reconstruction and reticulation analysis indicated that anthropophily most likely evolved once, involving adaptive introgression, in the early Pleistocene in Sundaland, giving rise to multiple descendent anthropophilic species. Such early origination of anthropophily must necessarily have been in response to the arrival of early hominins ( Homo erectus ) rather than anatomically modern humans, likely associated with loss and fragmentation of rainforests during the early Pleistocene. The early origination of anthropophily also provides independent non-archaeological evidence supporting the limited fossil record of early hominin colonization in Southeast Asia around 1.8 Mya.