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Ancient genome-wide admixture extends beyond the current hybrid zone between Macaca fascicularis and M. mulatta

Authors

  • NAOKI OSADA,

    1. Department of Biomedical Resources, National Institute of Biomedical Innovation, 7-6-8 Saito-Asagi, Ibraki, Osaka 567-0085, Japan
    2. Department of Population Genetics, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 441-8540, Japan
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  • YASUHIRO UNO,

    1. Pharmacokinetics and Bioanalysis Center, Shin Nippon Biomedical Laboratories, Ltd, 16-1 Minami-Akasaka, Kainan, Wakayama 642-0017, Japan
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  • KATSUHIKO MINETA,

    1. Graduate School of Information Science and Technology, Hokkaido University, N14W9 Sapporo 060-0814, Japan
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  • YOSUKE KAMEOKA,

    1. Department of Biomedical Resources, National Institute of Biomedical Innovation, 7-6-8 Saito-Asagi, Ibraki, Osaka 567-0085, Japan
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  • ICHIRO TAKAHASHI,

    1. Department of Biomedical Resources, National Institute of Biomedical Innovation, 7-6-8 Saito-Asagi, Ibraki, Osaka 567-0085, Japan
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  • KEIJI TERAO

    1. Tsukuba Primate Research Center, National Institute of Biomedical Innovation, 1 Hachimandai, Tsukuba 305-0843, Japan
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Fax: +81 (55) 981-6793; E-mail: nosada@lab.nig.ac.jp

Abstract

Macaca fascicularis and Macaca mulatta are two of the most commonly used laboratory macaques, yet their genetic differences at a genome-wide level remain unclear. We analysed the multilocus DNA sequence data of 54 autosomal loci obtained from M. fascicularis samples from three different geographic origins and M. mulatta samples of Burmese origin. M. fascicularis shows high nucleotide diversity, four to five times higher than humans, and a strong geographic population structure between Indonesian-Malaysian and Philippine macaques. The pattern of divergence and polymorphism between M. fascicularis and M. mulatta shows a footprint of genetic exchange not only within their current hybrid zone but also across a wider range for more than 1 million years. However, genetic admixture may not be a random event in the genome. Whereas randomly selected genic and intergenic regions have the same evolutionary dynamics between the species, some cytochrome oxidase P450 (CYP) genes (major chemical metabolizing genes and potential target genes for local adaptation) have a significantly larger species divergence than other genes. By surveying CYP3A5 gene sequences of more than a hundred macaques, we identified three nonsynonymous single nucleotide polymorphisms that were highly differentiated between the macaques. The mosaic pattern of species divergence in the genomes may be a consequence of genetic differentiation under ecological adaptation and may be a salient feature in the genomes of nascent species under parapatry.

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