Degree of genetic admixture in hybrid populations between macaca fascicularis fascicularis and M. F. aurea in association with stone tool-use behavior

Abstract

Burmese long-tailed macaque (Macaca fascicularis aurea) is the only Old World monkey that habitually uses stones as tools to access encased food. The natural range of M. f. aurea closely contacts to the common long-tailed macaque (M. f. fascicularis) in southern Thailand at 8°10'-12°24'N, where the intraspecific hybridization between the two subspecies was reported. While M. f. aurea x M. f. fascicularis hybrids were expressed a stone-tool use behavior, the behavior has never been seen in the wild or captive M. f. fascicularis. It is interesting to understand if the genetic factor plays a role on the emergence of this behavior. This study surveyed the populations of M. f. aurea, M. f. fascicularis and hybrids at the intraspecific hybrid zone and vicinity, identified morphological subspecies, observed/tested the stone-tool use behaviors, collected blood and fecal samples for genetic analyses, and genetic subspecies identification using mtDNA, Y-chromsome genes (SRY and TSPY), and autosomal single nucleotide polymorphism (SNP) derived from Restriction Site Associated DNA Sequencing (RADseq) as genetic markers. The findings in this study illustrated the influence of the early-middle Pleistocene transition (EMPT) on the split of M. f. aurea lineage through the southward migration from Myanmar/Bangladesh to southwestern Thailand. This study confirmed the previous hypothesis of the male-mediated intraspecific hybridization from M. f. aurea to M. f. fascicularis populations. In addition, the analysis of RADseq-derived SNPs indicated an asymmetrically (or unidirectionally) genetic introgression of M. f. aurea to M. f. fascicularis populations that occurred far beyond the previously reported intraspecific hybrid zone. The analysis of an association between the identified morphological subspecies or identified genetic subspecies and the stone-assisted behaviors, that were categorized into 4 levels; stone-tool use behavior, food pounding behavior, stone-play behavior and none, was performed. The statistically significant association between the morphologically identified M. f. aurea and hybrids and the complex stone-associated behaviors was detected, while it was no association between the identified genetic subspecies (based on mtDNA, SRY and TSPY) and the stone-associated behaviors. However, the SNP markers that indicate the degree of genetic admixture in hybrid populations can associate the high degree of M. f. aurea ancestry in M. fascicularis with stone-play and stone-tool use behaviors and the low degree of M. f. aurea ancestry in M. fascicularis with non-stone use behavior. Thus, these results imply the possibility of genetic influences on the emergence, the prevalence and the restriction of stone-tool use behavior in M. f. aurea and hybrids.