Evolutionary History of the Odd-Nosed Monkeys and the Phylogenetic Position of the Newly Described Myanmar Snub-Nosed Monkey Rhinopithecus strykeri

Abstract

Odd-nosed monkeys represent one of the two major groups of Asian colobines. Our knowledge about this primate group is still limited as it is highlighted by the recent discovery of a new species in Northern Myanmar. Although a common origin of the group is now widely accepted, the phylogenetic relationships among its genera and species, and the biogeographic processes leading to their current distribution are largely unknown. To address these issues, we have analyzed complete mitochondrial genomes and 12 nuclear loci, including one X chromosomal, six Y chromosomal and five autosomal loci, from all ten odd-nosed monkey species. The gene tree topologies and divergence age estimates derived from different markers were highly similar, but differed in placing various species or haplogroups within the genera Rhinopithecus and Pygathrix. Based on our data, Rhinopithecus represent the most basal lineage, and Nasalis and Simias form closely related sister taxa, suggesting a Northern origin of odd-nosed monkeys and a later invasion into Indochina and Sundaland. According to our divergence age estimates, the lineages leading to the genera Rhinopithecus, Pygathrix and Nasalis+Simias originated in the late Miocene, while differentiation events within these genera and also the split between Nasalis and Simias occurred in the Pleistocene. Observed gene tree discordances between mitochondrial and nuclear datasets, and paraphylies in the mitochondrial dataset for some species of the genera Rhinopithecus and Pygathrix suggest secondary gene flow after the taxa initially diverged. Most likely such events were triggered by dramatic changes in geology and climate within the region. Overall, our study provides the most comprehensive view on odd-nosed monkey evolution and emphasizes that data from differentially inherited markers are crucial to better understand evolutionary relationships and to trace secondary gene flow.

Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation

“…Regardless of the reference genomes and treebuilding methods used, the genome phylogeny strongly supported the interspecific relationships shown in a previous tree based on the analyses of several nuclear genes ( Fig. 1) and significantly rejected the relationships represented in a tree based on the mitochondrial genome 12 (P = 1 × 10 −40 in an approximately uniform test). Estimation of divergence times suggests that the two high-altitude 'Himalaya' species R. bieti and R. strykeri diverged from the lowland R. avunculus species 0.80 million years ago and that the high-altitude northern species R. roxellana separated from the lowland R. brelichi species 1.07 million years ago ( Fig.…”

“…We observed that the expression profiles of highly expressed genes from the digestive system (small intestine, large intestine, and stomach) and energyconsuming tissues (heart and skeletal muscle) were more similar in Phylogenetic relationships of the Rhinopithecus species inferred from a previous nuclear gene analysis 12 . The present whole-genome phylogeny supports the same relationships, regardless of the reference genomes and tree-building methods used.…”

Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history

“…Comparing orthologs between rhesus macaque and the snub-nosed monkeys, we reconstructed a maximum-likelihood phylogeny supporting the hypothesis of a separation between the northern species (R. roxellana and R. brelichi) and the 'Himalayan' species (R. bieti and R. strykeri) 25 with 100% bootstrap support values (Fig. 5a).…”

“…These times coincide with the uplift of the Tibetan plateau-Yuanmu movement (~1.6 million years ago)-which helped to create the higher mountains of the Himalayas 31 and might have resulted in the split of the northern and Himalayan species as well as the subsequent separation of R. roxellana and R. brelichi. Divergence within the Himalayan species appears to have begun about 0.3 million years ago, more recently than previously estimated 25 . The short branches of these lineages in the tree also imply that incomplete lineage sorting (ILS; cases where the gene tree was different from the species tree) and/or introgression have occurred within this clade.…”

“…The phylogenetic relationships within this group are controversial 25 , so we used short-read sequencing to address this question from a genome-wide perspective, carrying out wholegenome sequencing of the black-white (R. bieti), gray (R. brelichi) and Myanmar (R. strykeri) snub-nosed monkeys with approximately 30-fold coverage for each individual (~282 Gb in total) ( Supplementary Fig. 26 and Supplementary Tables 35-38).…”