State Key Laboratory for Conservation and Utilization of Bio-Resource in Yunnan, Yunnan University, Kunming, China.
School of Life Sciences, Yunnan University, Kunming, China.
Mol Biol Evol. 2019 Mar 1;36(3):487-499. doi: 10.1093/molbev/msy220.
The origin and population history of the endangered golden snub-nosed monkey (Rhinopithecus roxellana) remain largely unavailable and/or controversial. We here integrate analyses of multiple genomic markers, including mitochondrial (mt) genomes, Y-chromosomes, and autosomes of 54 golden monkey individuals from all three geographic populations (SG, QL, and SNJ). Our results reveal contrasting population structures. Mt analyses suggest a division of golden monkeys into five lineages: one in SNJ, two in SG, and two in QL. One of the SG lineages (a mixed SG/QL lineage) is basal to all other lineages. In contrast, autosomal analyses place SNJ as the most basal lineage and identify one QL and three SG lineages. Notably, Y-chromosome analyses bear features similar to mt analyses in placing the SG/QL-mixed lineage as the first diverging lineage and dividing SG into two lineages, while resembling autosomal analyses in identifying one QL lineage. We further find bidirectional gene flow among all three populations at autosomal loci, while asymmetric gene flow is suggested at mt genomes and Y-chromosomes. We propose that different population structures and gene flow scenarios are the result of sex-linked differences in the dispersal pattern of R. roxellana. Moreover, our demographic simulation analyses support an origin hypothesis suggesting that the ancestral R. roxellana population was once widespread and then divided into SNJ and non-SNJ (SG and QL) populations. This differs from previous mt-based "mono-origin (SG is the source population)" and "multiorigin (SG is a fusion of QL and SNJ)" hypotheses. We provide a detailed and refined scenario for the origin and population history of this endangered primate species, which has a broader significance for Chinese biogeography. In addition, this study highlights the importance to investigate multiple genomic markers with different modes of inheritance to trace the complete evolutionary history of a species, especially for those exhibiting differential or mixed patterns of sex dispersal.
受威胁的金丝猴(Rhinopithecus roxellana)的起源和种群历史在很大程度上尚不清楚和/或存在争议。我们综合分析了来自三个地理种群(SG、QL 和 SNJ)的 54 只金丝猴个体的多个基因组标记,包括线粒体(mt)基因组、Y 染色体和常染色体。我们的研究结果揭示了截然不同的种群结构。mt 分析表明,金丝猴分为五个谱系:一个在 SNJ,两个在 SG,两个在 QL。SG 的一个谱系(SG/QL 混合谱系)是所有其他谱系的基础。相比之下,常染色体分析将 SNJ 作为最基础的谱系,并确定了一个 QL 和三个 SG 谱系。值得注意的是,Y 染色体分析在将 SG/QL 混合谱系作为第一个分支谱系进行划分方面与 mt 分析相似,并将 SG 分为两个谱系,而在识别一个 QL 谱系方面与常染色体分析相似。我们还发现所有三个种群的常染色体基因座存在双向基因流,而 mt 基因组和 Y 染色体则存在不对称基因流。我们提出,不同的种群结构和基因流情景是金丝猴扩散模式的性连锁差异的结果。此外,我们的人口统计模拟分析支持一个起源假说,即该物种的祖先 R. roxellana 种群曾经分布广泛,然后分为 SNJ 和非-SNJ(SG 和 QL)种群。这与之前基于 mt 的“单一起源(SG 是源种群)”和“多起源(SG 是 QL 和 SNJ 的融合)”假说不同。我们为这个濒危灵长类物种的起源和种群历史提供了一个详细而精细的情景,这对中国生物地理学具有更广泛的意义。此外,这项研究强调了调查具有不同遗传模式的多个基因组标记以追踪一个物种的完整进化历史的重要性,特别是对于那些表现出不同或混合性别扩散模式的物种。