Genetic diversity of long-tailed macaque macaca fascicularis and rhesus macaque M. mulatta: mainly focus on their hybridization range

Abstract

Macaca fascicularis fascicularis (Mff) are one of the most popularly used non-human primate models in biomedical research and thus their genetic characteristics are a focal point of interest. However, Mff live parapatrically with M. mulatta (Mm) at 15-20° N and with M. fascicularis aurea (Mfa) at 8-12° N in Thailand and became hybridized. Using mtDNA, Y-chromosome and SNPs genetic markers, this study aims to determine the hybridization at interspecific (Mff x Mm) and intersubspecific (Mff x Mfa) levels of the Mff originated from Thailand and vicinity. Based on the mtDNA and Y-chromosome phylogenies, it indicated that hybridization between Mm and Mff was driven uni-directionally by the introgression of Mm males into Mff populations. The Mm gene flow directed southward and was restricted south of the Isthmus of Kra between SSD (Chumphon) and WSK (Phang-nga). In contrast, SNP genotyping revealed a bi-directional hybridization where genetic introgression was either from Mm into Mff or vice versa, however the gene flow from Mm into Mff was far greater (~10° latitude of distant) than from Mff into Mm (~4° latitude). This caused the Mm gene flow far beyond the Isthmus of Kra which proposed to terminate somewhere between the KN/KTK (Songkla) and Singapore/Sarawak. The migration scenario of Mff across land bridge during the glacial and interglacial cycles was also proposed based on the mtDNA phylogeny as well as changes of zoogeographical barriers. Based on the mtDNA and Y-chromosome phylogenies, the Mff x Mfa hybrids were subdivided into two groups; Indochinese (SRY, KRI, WKC, and BMS) and Sundaic (SRI) hybrids. Two hybridization scenarios were proposed. One is that Mfa males migrated from mainland Myanmar southward along Mergui archipelago toward the Andaman sea coast, introgressed into Mff populations and formed the Sundaic Mff x Mfa hybrids. Another is that some Mfa males migrated northeastward across the low altitude area of the Dawna range to the Thai Gulf, while they were along Mergui Archipelago, introgressed into Mff populations and formed the Indochinese Mff x Mfa hybrid. Since Mfa clade was separated from the Mff-Mm clade in mtDNA phylogenetic tree and it is the only one of 22 macaque species performing stone tool using behavior, the taxonomic status of this subspecies is now being questioned. In conclusion, this study unravels a complexity in Mff genomes based on their evolutionary history and hybridizations either with Mm or Mfa. Thus, the selection and use of Mff for biomedical research should consider not only species or subspecies identification, but also their origins.