Abstract
The evolutionary history of macaques, genus Macaca, has been under debate due to the short times of divergence. In this study, maternal, paternal, and biparental genetic systems were applied to infer phylogenetic relationships among macaques and to trace ancient hybridization events in their evolutionary history. Using a PCR display method, 17 newly phylogenetically informative Alu insertions were identified from M. assamensis. We combined presence/absence analysis of 84 Alu elements with mitochondrial genomes as well as nuclear sequences (five autosomal genes, two Y chromosomal genes, and one X chromosomal fragment) to reconstruct a robust macaque phylogeny. Topologies generated from different inherited markers were similar supporting six well defined species groups and a close relationship of M. assamensis and M. thibetana, but differed in the placing of M. arctoides. Both Alu elements and nuclear genes supported that M. arctoides was close to the sinica group, whereas the mitochondrial data clustered it into the fascicularis/mulatta lineage. Our results reveal that a sex-biased hybridization most likely occurred in the evolutionary history of M. arctoides, and suggest an introgressive pattern of male-mediated gene flow from the ancestors of M. arctoides to the M. mulatta population followed by nuclear swamping. According to the estimation of divergence dates, the hybridization occurred around 0.88~1.77 mya (nuclear data) or 1.38~2.56 mya (mitochondrial data). In general, our study indicates that a combination of various molecular markers could help explain complicated evolutionary relationships. Our results have provided new insights into the evolutionary history of macaques and emphasize that hybridization might play an important role in macaque evolution.
Highlights
Macaques represent one of the most successful primate radiations with 20–23 extant species in genus Macaca
Combining a computational approach and a PCR display method, we identified phylogenetically informative Alu loci from M. assamensis
By combining presence/absence pattern of Alu elements with autosomal, Y chromosomal, X chromosomal sequences, and the mitochondrial genome, our study provides comprehensive insights into the evolutionary history of macaque species
Summary
Macaques represent one of the most successful primate radiations with 20–23 extant species in genus Macaca. With the exception of M. sylvanus in North Africa and Southern Europe, macaques are widely distributed in southern and eastern Asia [4], ranking second only to the world-wide distribution of humans among the extant primates. With such a variety of habitats and species that differ in ecology and external morphology, macaques are best known as a prime group for studies of species radiation and evolution as well as an important animal model in medical research. It is important to elucidate the phylogeny of the extant taxa of macaques, which will contribute to our understanding of the evolutionary history of the genus as well as other primate radiations
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