Taxonomy, Evolutionary and Dispersal Events of Pig-Tailed Macaque, Macaca nemestrina (Linnaeus, 1766) in Southeast Asia with Description of a New Subspecies, Macaca nemestrina perakensis in Malaysia

Abstract

The pig-tailed macaque, Macaca nemestrina, which is distributed in Peninsular Malaysia, Thailand, Borneo, and Sumatra, has been the subject of unstable and changing taxonomic entity in the M. nemestrina group. This species is involved with a human-macaque conflict in Malaysia and at the same time played an important role in the ethnozoological culture of Malaysian. Even so, comprehensive phylogenetic, population genetics and biogeographical analysis of M. nemestrina in Malaysia are non-existent after decades of intensive research on the genus itself. Thus, we conducted the first comprehensive genetic study of M. nemestrina in Malaysia, based on three mitochondrial loci-Cytochrome b (567 bp), D-loop (398 bp), and COI (577 bp)-from 27 individuals representing Malaysia, plus an additional 26 sequences of Southeast Asian macaques from Genbank. Comparative biogeographical analysis in this study supports the positions of M. nemestrina in M. nemestrina groups as opposed to the silenus or Sulawesi groups. Results from this study also indicate that Bornean populations are the first extant lineages to separate from the other examined lineages of M. nemestrina, M. leonina, M. pagensis, and M. siberu in Southeast Asia. Molecular clock analysis suggested that M. nemestrina arrived in the Malay Peninsula about 0.32 million years ago (MYA). Our results indicate that the population of pig-tailed macaque from Perak (west Peninsular Malaysia) differs genetically based on all phylogenetic and population genetic analyses. Morphologically, Perak's pig-tailed macaque shows brighter coloration than M. n. nemestrina. Thus, we proposed a new subspecies for Perak's pig-tailed macaque as Macaca nemestrina perakensis distributed in the state of Perak, Peninsular Malaysia. This research helps resolve the taxonomic position and population genetics of pig-tailed macaque in Malaysia, which contribute directly to conservation and management of the species in Malaysia.

Keywords: Cercopithecinae; Macaca nemestrina; Phylogeography; Pig-tailed macaque; Taxonomy.

Fig. 1.

Neighbor-Joining phylogenetic tree reconstructed based on Kimura-2-Parameter for three loci (Cyt b, D-loop and COI) with 1000 bootstrap replications. Bootstrap values indicated on the nodes.

Fig. 2.

Maximum Parsimony phylogenetic tree reconstructed for three loci (Cyt b, D-loop and COI) based on tree bisection and reconnection (TBR) algorithms, heuristic searching method, 1,000 random stepwise additions and 1,000 bootstrap replications. Bootstrap values indicated on the nodes.

Fig. 3.

Bayesian inference of the 50% majority rule consensus tree for three loci (Cyt b, D-loop and COI) with bayesian posterior probability (PP) accordingly indicated on the branch.

Fig. 4.

Molecular divergence tree of the Cyt b sequence of Southeast Asia’s M. nemestrina, M. pagensis, M. siberu, and M. leonina with the numbers on the nodes representing divergence time in millions of years (MYA) and PP in parentheses indicating the confidence interval.

Fig. 5.

Minimum Spanning Network (MSN) illustrating haplotype relationships among M. nemestrina’s populations based on Cyt b, D-loop and COI sequences.

Fig. 6.

Mismatch distribution of expected and observed frequencies of pairwise differences among Cyt b, D-loop and COI sequences for M. nemestrina population in Malaysia.

Fig. 7.

Hypothetical biogeographical scenario proposed for dispersal events of M. nemestrina in Southeast Asia.

Fig. 8.

Morphological differences between M. n. nemestrina, M. n. perakensis and M. leonina (Pictures of M. leonina adapted from Malaivijitnond et al. 2012).