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Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques

Smith DG, McDonough JW, George DA

Am J Primatol, 2007 Feb;69(2):182-98.
PMID: 17177314

An 835 base pair (bp) fragment of mitochondrial DNA (mtDNA) was sequenced to characterize genetic variation within and among 1,053 samples comprising five regional populations each of longtail macaques (Macaca fascicularis) and rhesus macaques (Macaca mulatta), and one sample each of Japanese (M. fuscata) and Taiwanese (M. cyclopis) macaques. The mtDNA haplotypes of longtail macaques clustered in two large highly structured clades (Fas1 and Fas2) of a neighbor-joining tree that were reciprocally monophyletic with respect to those representing rhesus macaques, Japanese macaques, and Taiwanese macaques. Both clades exhibited haplotypes of Indonesian and Malaysian longtail macaques widely dispersed throughout them; however, longtail macaques from Indochina, Philippines, and Mauritius each clustered in a separate well-defined clade together with one or a few Malaysian and/or Indonesian longtail macaques, suggesting origins on the Sunda shelf. Longtail macaques from Malaysia and Indonesia were far more genetically diverse, and those from Mauritius were far less diverse than any other population studied. Nucleotide diversity between mtDNA sequences of longtail macaques from different geographic regions is, in some cases, greater than that between Indian and Chinese rhesus macaques. Approximately equal amounts of genetic diversity are due to differences among animals in the same regional population, different regional populations, and different species. A greater proportion of genetic variance was explained by interspecies differences when Japanese and Taiwanese macaques were regarded as regional populations of rhesus macaques than when they were treated as separate species. Rhesus macaques from China were more closely related to both Taiwanese and Japanese macaques than to their own conspecifics from India.
Fulltext Two New Moray Eels of Genera Diaphenchelys and Gymnothorax (Anguilliformes: Muraenidae) from Taiwan and the Philippines

Huang WC, Smith DG, Loh KH, Liao TY

Zool Stud, 2021;60:e24.
PMID: 34853614 DOI: 10.6620/ZS.2021.60-24

Two new moray eels of the genera Diaphenchelys and Gymnothorax from Taiwan and the Philippines are described. Diaphenchelys laimospila sp. nov. is described based on two specimens that represent the third species and a new geographic record of the genus. It can be distinguished from the other two congeners by the number of cephalic sensory pores, vertebral formula, morphometric measurements, and the coloration pattern. Gymnothorax pseudokidako sp. nov. is a muraenid with a dark brown body covered by pale snowflake-like blotches. It differs from the most similar species Gymnothorax kidako (Temminck and Schlegel) by having a relatively short tail (50.5-53.0% vs. 52.9-56.4% of TL), more dentary teeth (17-26 vs. 16-20), fewer total vertebrae (134-139 vs. 137-143), and the absence of white margin on anal fin (vs. prominent white margin). These two new species were also confirmed by molecular analyses, the mitochondrial COI gene (593 bp) for D. laimospila, and the nuclear EGR3 gene (767 bp) for G. pseudokidako.
Annotated checklist of eels (orders Anguilliformes and Saccopharyngiformes) from Taiwan

Ho HC, Smith DG, Mccosker JE, Hibino Y, Loh KH, Tighe KA, et al.

Zootaxa, 2015;4060:140-89.
PMID: 26701598 DOI: 10.11646/zootaxa.4060.1.16

An annotated checklist of eels, orders Anguilliformes and Saccopharyngiformes, occurring in Taiwanese waters is presented. The checklist is the result of a series of systematic studies conducted by the authors in the past few years. The eel fauna of Taiwan is one of the richest in the world with a total of 206 species in 74 genera and 13 families in Anguilliformes and a single species in Saccopharyngiformes. The most species-rich families are the Muraenidae with 71 species, followed by the Ophichthidae with 60 species, the Congridae with 29 species, and the Synaphobranchidae with 17 species. Moreover, three genera and 42 species have been described based on at least one type specimen collected from Taiwan. Of these, 36 species are recognized as valid and 23 species are known only from Taiwanese waters at present. Historical records of all Taiwanese eel species are reviewed by examining the original descriptions and figures, vouchers, as well as the recently collected specimens, where available. This represents the first detailed checklist of eels from Taiwanese waters.
Fulltext A genetic comparison of two alleged subspecies of Philippine cynomolgus macaques

Smith DG, Ng J, George D, Trask JS, Houghton P, Singh B, et al.

Am. J. Phys. Anthropol., 2014 Sep;155(1):136-48.
PMID: 24979664 DOI: 10.1002/ajpa.22564

Two subspecies of cynomolgus macaques (Macaca fascicularis) are alleged to co-exist in the Philippines, M. f. philippensis in the north and M. f. fascicularis in the south. However, genetic differences between the cynomolgus macaques in the two regions have never been studied to document the propriety of their subspecies status. We genotyped samples of cynomolgus macaques from Batangas in southwestern Luzon and Zamboanga in southwestern Mindanao for 15 short tandem repeat (STR) loci and sequenced an 835 bp fragment of the mtDNA of these animals. The STR genotypes were compared with those of cynomolgus macaques from southern Sumatra, Singapore, Mauritius and Cambodia, and the mtDNA sequences of both Philippine populations were compared with those of cynomolgus macaques from southern Sumatra, Indonesia and Sarawak, Malaysia. We conducted STRUCTURE and PCA analyses based on the STRs and constructed a median joining network based on the mtDNA sequences. The Philippine population from Batangas exhibited much less genetic diversity and greater genetic divergence from all other populations, including the Philippine population from Zamboanga. Sequences from both Batangas and Zamboanga were most closely related to two different mtDNA haplotypes from Sarawak from which they are apparently derived. Those from Zamboanga were more recently derived than those from Batangas, consistent with their later arrival in the Philippines. However, clustering analyses do not support a sufficient genetic distinction of cynomolgus macaques from Batangas from other regional populations assigned to subspecies M. f. fascicularis to warrant the subspecies distinction M. f. philippensis.
Genetic analysis of samples from wild populations opens new perspectives on hybridization between long-tailed (Macaca fascicularis) and rhesus macaques (Macaca mulatta)

Bunlungsup S, Kanthaswamy S, Oldt RF, Smith DG, Houghton P, Hamada Y, et al.

Am J Primatol, 2017 12;79(12).
PMID: 29095514 DOI: 10.1002/ajp.22726

In the past decade, many researchers have published papers about hybridization between long-tailed and rhesus macaques. These previous works have proposed unidirectional gene flow with the Isthmus of Kra as the zoogeographical barrier of hybridization. However, these reports analyzed specimens of unknown origin and/or did not include specimens from Thailand, the center of the proposed area of hybridization. Collected specimens of long-tailed and rhesus macaques representing all suspected hybridization areas were examined. Blood samples from four populations each of long-tailed and rhesus macaques inhabiting Thailand, Myanmar, and Laos were collected and analyzed with conspecific references from China (for rhesus macaques) and multiple countries from Sundaic regions (for long-tailed macaques). Ninety-six single nucleotide polymorphism (SNP) markers specifically designed to interrogate admixture and ancestry were used in genotyping. We found genetic admixture maximized at the hybrid zone (15-20°N), as well as admixture signals of varying strength in both directions outside of the hybrid zone. These findings show that the Isthmus of Kra is not a barrier to gene flow from rhesus to long-tailed populations. However, to precisely identify a southernmost barrier, if in fact a boundary rather than simple isolation by distance exists, the samples from peninsular Malaysia must be included in the analysis. Additionally, a long-tailed to rhesus gene flow boundary was found between northern Thailand and Myanmar. Our results suggest that selection of long-tailed and rhesus macaques, the two most commonly used non-human primates for biomedical research, should take into account not only the species identification but also the origin of and genetic admixture within and between the species.
Fulltext Distribution and prevalence of malaria parasites among long-tailed macaques (Macaca fascicularis) in regional populations across Southeast Asia

Zhang X, Kadir KA, Quintanilla-Zariñan LF, Villano J, Houghton P, Du H, et al.

Malar J, 2016 09 02;15(1):450.
PMID: 27590474 DOI: 10.1186/s12936-016-1494-0

BACKGROUND: Plasmodium knowlesi and Plasmodium cynomolgi are two malaria parasites naturally transmissible between humans and wild macaque through mosquito vectors, while Plasmodium inui can be experimentally transmitted from macaques to humans. One of their major natural hosts, the long-tailed macaque (Macaca fascicularis), is host to two other species of Plasmodium (Plasmodium fieldi and Plasmodium coatneyi) and is widely distributed in Southeast Asia. This study aims to determine the distribution of wild macaques infected with malarial parasites by examining samples derived from seven populations in five countries across Southeast Asia.
METHODS: Plasmodium knowlesi, P. cynomolgi, P. coatneyi, P. inui and P. fieldi, were detected using nested PCR assays in DNA samples from 276 wild-caught long-tailed macaques. These samples had been derived from macaques captured at seven locations, two each in the Philippines (n = 68) and Indonesia (n = 70), and one each in Cambodia (n = 54), Singapore (n = 40) and Laos (n = 44). The results were compared with previous studies of malaria parasites in long-tailed macaques from other locations in Southeast Asia. Fisher exact test and Chi square test were used to examine the geographic bias of the distribution of Plasmodium species in the macaque populations.
RESULTS: Out of 276 samples tested, 177 were Plasmodium-positive, with P. cynomolgi being the most common and widely distributed among all long-tailed macaque populations (53.3 %) and occurring in all populations examined, followed by P. coatneyi (20.4 %), P. inui (12.3 %), P. fieldi (3.4 %) and P. knowlesi (0.4 %). One P. knowlesi infection was detected in a macaque from Laos, representing the first documented case of P. knowlesi in wildlife in Laos. Chi square test showed three of the five parasites (P. knowlesi, P. coatneyi, P. cynomolgi) with significant bias in prevalence towards macaques from Malaysian Borneo, Cambodia, and Southern Sumatra, respectively.
CONCLUSIONS: The prevalence of malaria parasites, including those that are transmissible to humans, varied among all sampled regional populations of long-tailed macaques in Southeast Asia. The new discovery of P. knowlesi infection in Laos, and the high prevalence of P. cynomolgi infections in wild macaques in general, indicate the strong need of public advocacy in related countries.
Fulltext Ancestry, Plasmodium cynomolgi prevalence and rhesus macaque admixture in cynomolgus macaques (Macaca fascicularis) bred for export in Chinese breeding farms

Zhang X, Meng Y, Houghton P, Liu M, Kanthaswamy S, Oldt R, et al.

J Med Primatol, 2017 04;46(2):31-41.
PMID: 28266719 DOI: 10.1111/jmp.12256

BACKGROUND: Most cynomolgus macaques (Macaca fascicularis) used in the United States as animal models are imported from Chinese breeding farms without documented ancestry. Cynomolgus macaques with varying rhesus macaque ancestry proportions may exhibit differences, such as susceptibility to malaria, that affect their suitability as a research model.
METHODS: DNA of 400 cynomolgus macaques from 10 Chinese breeding farms was genotyped to characterize their regional origin and rhesus ancestry proportion. A nested PCR assay was used to detect Plasmodium cynomolgi infection in sampled individuals.
RESULTS: All populations exhibited high levels of genetic heterogeneity and low levels of inbreeding and genetic subdivision. Almost all individuals exhibited an Indochinese origin and a rhesus ancestry proportion of 5%-48%. The incidence of P. cynomolgi infection in cynomolgus macaques is strongly associated with proportion of rhesus ancestry.
CONCLUSIONS: The varying amount of rhesus ancestry in cynomolgus macaques underscores the importance of monitoring their genetic similarity in malaria research.