Mitogenomic phylogeny of the common long-tailed macaque (Macaca fascicularis fascicularis)

Background

Long-tailed macaques (Macaca fascicularis) are an important model species in biomedical research and reliable knowledge about their evolutionary history is essential for biomedical inferences. Ten subspecies have been recognized, of which most are restricted to small islands of Southeast Asia. In contrast, the common long-tailed macaque (M. f. fascicularis) is distributed over large parts of the Southeast Asian mainland and the Sundaland region. To shed more light on the phylogeny of M. f. fascicularis, we sequenced complete mitochondrial (mtDNA) genomes of 40 individuals from all over the taxon’s range, either by classical PCR-amplification and Sanger sequencing or by DNA-capture and high-throughput sequencing.

Results

Both laboratory approaches yielded complete mtDNA genomes from M. f. fascicularis with high accuracy and/or coverage. According to our phylogenetic reconstructions, M. f. fascicularis initially diverged into two clades 1.70 million years ago (Ma), with one including haplotypes from mainland Southeast Asia, the Malay Peninsula and North Sumatra (Clade A) and the other, haplotypes from the islands of Bangka, Java, Borneo, Timor, and the Philippines (Clade B). The three geographical populations of Clade A appear as paraphyletic groups, while local populations of Clade B form monophyletic clades with the exception of a Philippine individual which is nested within the Borneo clade. Further, in Clade B the branching pattern among main clades/lineages remains largely unresolved, most likely due to their relatively rapid diversification 0.93-0.84 Ma.

Conclusions

Both laboratory methods have proven to be powerful to generate complete mtDNA genome data with similarly high accuracy, with the DNA-capture and high-throughput sequencing approach as the most promising and only practical option to obtain such data from highly degraded DNA, in time and with relatively low costs. The application of complete mtDNA genomes yields new insights into the evolutionary history of M. f. fascicularis by providing a more robust phylogeny and more reliable divergence age estimations than earlier studies.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1437-0) contains supplementary material, which is available to authorized users.     

Prenatal growth in the cynomolgus and rhesus macaque (Macaca fascicularis and Macaca mulatta): A comparison by ultrasonography

The rhesus monkey has played an important role in the history of reproductive research. Because of limitations on the exportation and availability of this species, several other species of nonhuman primates have been considered as alternate models. Among them is the crab-eating, or cynomolgus, macaque (Macaca fascicularis), which displays similarities in developmental, reproductive, and physiological parameters. The use of both species of macaques for pregnancy-related studies necessitates the assessment of differences in growth and development through gestation. Observations during the embryonic and fetal periods in both species have been compared with diagnostic ultrasound. Results indicate no significant differences in size during the embryonic and early fetal periods, but a greater acceleration of growth in the rhesus begins at approximately 100–110 gestational days (GD). Analysis of embryonic and fetal heart rates indicate no differences between the two species. Normal predictive values for a variety of growth parameters including gestational sac, greatest length, biparietal diameter, and femur length have boon calculated by multiple regression analysis. These charts have proven useful for confirming the gestational age after timed matings and for predicting the age of animals for which the conception date is not known.     

Use of ultrasound for early pregnancy detection in the rhesus and cynomolgus macaque (Macaca mulatta and Macaca fascicularis)

Diagnostic ultrasound provides an accurate method for the detection of early pregnancy and embryonic loss in macaque species. A developing gestational sac (GS) may be observed on gestational day (GD) 14-15 with positive identification on GD 16-18. Visualization of the yolk sac, embryo, and developing heart on GD 21-25 confirms pregnancy. Continuous observations during embryogenesis provide useful information when assessing the teratogenic potential of a variety of agents.     

Hematologic reference values for the fetal long-tailed macaque (Macaca fascicularis)

Complete blood counts (CBCs) were performed on 68 fetal macaque blood samples collected from 31 fetuses by repeat ultrasound-guided cardiocentesis (gestational day [GD] 80–150; term ～ GD 165) with the goal of defining normative hematologic reference values during prenatal life. Lymphocytes were the primary white blood cells (WBCs) observed throughout gestation. Segmented neutrophils were the second highest percent of WBCs and were noted to rise significantly during GD 130–140. Overall, WBCs increased progressively throughout gestation with a transient decline at the beginning of the third trimester (～ GD 110). A steady linear rise in red blood cells (RBCs), hemoglobin, and hematocrit was observed with a marginal decline close to term; mean corpuscular hemoglobin (MCH) and mean corpuscular volume (MCV) showed a consistent linear decline throughout gestation whereas mean corpuscular hemoglobin concentration (MCHC) remained relatively stable. Nucleated RBCs (NRBCs per 100 WBCs) were present on GD 80, showed a sharp decline mid-second trimester (～ GD 90), and were significantly diminished by the beginning of the third trimester (～ GD 110). No quantitative changes in platelets were noted throughout the study period. Evaluations of erythrocyte morphology indicated polychromasia and anisocytosis as typical characteristics throughout gestation with rare occurrence of hypochromasia and poikilocytosis. Howell-Jolly bodies were intermittently observed. These data reveal distinct similarities when compared to prenatal hematologic characteristics for human fetuses and provide baseline data which can be applied to experimental studies where prenatal hematopoietic/hematologic toxicity may be anticipated. © 1993 Wiley-Liss, Inc.     

Developmental toxicity of temafloxacin hydrochloride in the long-tailed macaque (Macaca fascicularis)

The potential developmental toxicity of temafloxacin hydrochloride was studied in the long-tailed macaque (Macaca fascicularis). Ten animals in each of the three drug-treated groups (25, 50, and 100 mg/kg) were administered temafloxacin via nasogastric intubation during gestational days (GD) 20-50. A control group of ten animals received vehicle only. The dams were monitored daily for adverse physical signs and maternal blood samples were collected for analyses of serum progesterone (P), 17 beta-estradiol (E2), and chorionic gonadotropin (CG). In addition, the conceptus was monitored periodically by ultrasound during gestation to confirm growth and viability. Increased maternal toxicity (weight loss, anorexia, emesis) and embryolethality were observed at 100 mg/kg, and a no-observable-adverse-effect-level (NOAEL) of 50 mg/kg was established. The incidence of prenatal mortality was as follows: Control = 1/10 (10%); 25 mg/kg = 1/10 (10%); 50 mg/kg = 2/10 (20%); and 100 mg/kg = 5/10 (50%). Analysis of P, E2, and CG indicated no significant effect of treatment. In addition, no significant differences were observed in embryonic/fetal growth and development when compared to historical controls. No gross structural changes were observed in fetuses exposed to 50 or 100 mg/kg, although one fetus exposed to 25 mg/kg exhibited microphthalmia. This anomaly was considered spontaneous and, therefore, unrelated to treatment.     

Intrauterine insemination with ultrasound guidance in the long-tailed macaque (Macaca fascicularis)

Techniques used for the artificial insemination of macaques have primarily involved instillation of the ejaculate into the vagina or cervical canal. Intrauterine insemination has been performed previously but only as a surgical procedure. The application of ultrasound-guided techniques for this purpose provides a method for efficiently inseminating macaques in a relatively noninvasive fashion. This report describes the successful transabdominal ultrasound-guided insemination of the long-tailed macaque and the potential application of this procedure to a variety of nonhuman primate species.     

Mixed cryoglobulinaemia in a rhesus macaque (Macaca mulatta)

We report cryoglobulinaemia (CG) in a rhesus macaque whose serum sample was gel‐like at <37°C and resolubilised upon warming. Mixed CG was diagnosed using serum protein electrophoresis and serum immunofixation electrophoresis. Renal damage and arthrophyma were observed during necropsy. This is the first report of CG in a non‐human primate.     

Feeding ecology of the long-tailed macaque(Macaca fascicularis) in Kalimantan Tengah,Indonesia

I studied long- tailed macaque (Macaca fascicularis)feeding behavior and ecology as part of a larger behavioral ecological study at the Natai Lengkuas Station, Tanjung Puting National Park, Kalimantan Tengah, Indonesia. I collected data on feeding behavior via scan sampling of all visible individuals in the focal group (approximately 800 observation hours). I established vegetational plots and monitored them monthly to determine food availability and abundance. I found long- tailed macaques to be primarily frugivorous;leaves, flowers, insects and bark provided the remainder of the diet. They used at least 33 plant species as food sources, but >60% of the diet was provided by only 5 species. Based on previous vegetational analyses, these tree species were among the highest in relative density. However, selection ratios for 19 food species indicate that 13 of them were selected more often than expected. Long- tailed macaques appear to be selective feeders but can exploit a variety of food sources during periods of food scarcity.     

Colonic adenocarcinoma in a rhesus macaque (Macaca mulatta)

Abstract: A spontaneous colonic adenocarcinoma and endometriosis was diagnosed in a 34-year-old female rhesus macaque (Macaca mulatta). The tumor caused partial obstruction of the ascending colon and histologically resembled the commonly described napkin-ring tumors of the descending and sigmoid colon found in humans. Serum levels of CA 125, a high-molecular-weight glycoprotein antigen that has been reported elevated in a variety of pathological conditions of the pelvic cavity in humans, was severely elevated. Both the adenocarcinoma and the endometriosis may have contributed to this finding.     

Subcutaneous hemangiosarcomas in a rhesus macaque (Macaca mulatta)

Hemangiosarcoma is a malignant tumor of vascular endothelial cell origin. The occurrence of hemangiosarcoma in nonhuman primates has been rarely documented. An adult male rhesus monkey was reported having a firm subcutaneous swelling, approximately 4.5 cm in diameter, on the ventral midline of the abdomen. Fine-needle aspiration, microbial culture, biopsy, radiographs, exploratory laparotomy, histopathology, immunohistochemistry, hematology, and serology were performed. A second subcutaneous mass approximately 4.5 x 4.0 x 2.7 cm developed on the ventral midline several weeks later. A fine-needle aspirate of the first mass consisted of numerous erythrocytes with few polymorphonuclear cells and lymphocytes. Histopathology showed foci of spindle-shaped cells surrounding the vascular spaces. Many spindle-shaped cells had prominent nucleoli, and mitotic figures could occasionally be seen. Immunohistochemical staining of the masses for Factor VIII-related antigen, an endothelial cell and tumor marker, yielded positive results. Both masses were consistent with hemangiosarcoma.     

Gastric trichobezoars in a rhesus macaque (Macaca mulatta)

On physical examination, a 5 x 10-cm abdominal mass was found in an eight-year-old female rhesus macaque. Radiography revealed an opaque mass in the cranial portion of the abdomen, displacing the stomach craniad. Percutaneous biopsy obtained hair with little tissue, confirming a diagnosis of trichobezoar. Initially, the hairball was medically managed by oral administration of lubricants. Medical management proved unsuccessful, the macaque began to lose weight, and two gastric trichobezoars were subsequently removed surgically. Normal appetite and activity were regained within one week. Gastric trichobezoars may lead to severe clinical illness, and should be considered in the differential diagnosis for anorexia and/or weight loss in any nonhuman primate. Trichobezoars may also be detected and treated prior to development of illness.     

Abdominal cysticercosis in a rhesus macaque (Macaca mulatta)

A mid-abdominal mass was discovered during routine physical examination of a rhesus macaque (Macaca mulatta). Further diagnostics and exploratory laparotomy were performed, revealing a fluid-filled cyst attached to the caudal free margin of the greater omentum. Formation and pulsatile movement of white-colored circumferential bands within the wall of the cyst were observed during surgery. The cyst was removed and later was dissected. The discovery of a single invaginated scolex identified the cyst as a cysticercus. The location and characteristics of the cysticercus were consistent with the larval form of Taenia hydatigena.     

Holoprosencephaly in a long-tailed macaque (Macaca fascicularis): A case report

A long-tailed macaque fetus with ethmocephaly, alobar holoprosencephaly, and arhinia is reported. This fetus was exposed to an antiprogestational agent, RU 486 (2.5 mg/kg intramuscular, once daily), during gestational days 15–18. Three hypotheses are proposed to explain these malformations: (1) they are a direct result of drug exposure, (2) they are a secondary effect of treatment and the result of decreased blood supply to the developing embryo due to an incomplete abortion, and (3) they represent a spontaneous occurrence.     

Spontaneous telangiectatic osteosarcoma in a rhesus macaque (Macaca mulatta)

Osteosarcoma (OS) is the most common type of bone cancer, especially in young. Telangiectatic osteosarcoma (TO) is a rare variant of OS, and hence, its occurrence, presentation, and prognosis are poorly understood. A 4‐year‐old female rhesus monkey presenting lameness and swelling was examined for a mass on the right humerus. Radiography revealed fracture and disorganized structure of bone tissue. Histopathological examination revealed malignant neoplasm composed of anaplastic osteoblasts, which invaded the bone marrow and surrounded blood‐filled cysts in the epiphysis and diaphysis forming septa. Cytogenetic analysis showed aneuploid cells, supernumerary AgNORs, and a marker fragment. The neoplasm was diagnosed as TO. To our knowledge, the occurrence of TO and its cytogenetic analysis were reported for the first time in non‐human primates.     

Pediatric hepatic hemangiosarcoma in a rhesus macaque (Macaca mulatta)

Background  Pediatric hepatic angiosarcoma is a rare condition in children with poor prognosis. Microscopically this neoplasm has a particular 'Kaposi-form' arrangement. Hemangiosarcoma in non-human primates is a rare finding.
Methods  Gross and microscopic examination of a 3-year-old rhesus were performed. Immunohistochemistry was used to characterize the hepatic hemangiosarcoma.
Results  The gross necropsy revealed hemoabdomen and a 4 × 3 × 3 cm mass in the liver with multiple smaller masses throughout the hepatic parenchyma. Histopathology confirmed a poorly differentiated hemangiosarcoma. Other organs submitted were free of metastases.
Conclusions  Hemangiosarcoma in non-human primates has been rarely reported. Diagnosis was confirmed by expression of endothelial-specific markers CD31 and vWF by immunohistochemistry. Due to the young age of this monkey and the particular solid pattern throughout the mass this neoplasm resembles pediatric hepatic angiosarcoma in humans.     

Lacrimal gland myoepithelioma in a rhesus macaque (Macaca mulatta)

An 18-year-old rhesus macaque (Macaca mulatta) developed ptosis of the left upper eyelid due to a mass that had first been observed 10 years previously. The 11 x 7 x 7-mm mass was surgically excised, and the ptosis resolved after 5 days. Histologic examination of the mass revealed two confluent cell populations. Most cells were spindle-shaped and were arranged in loose fascicles. Smaller numbers of cells had squamous differentiation. The spindle-shaped cells expressed smooth muscle actin. Cells with squamous differentiation did not express smooth muscle actin, but did, along with around half of the spindle-shaped cells, express pan-cytokeratin. On the basis of histologic and immunohistochemical findings, the mass was diagnosed as myoepithelioma. The neoplasm most likely originated from the palpebral lobe of the lacrimal gland, although accessory lacrimal gland origin could not be excluded. Recurrence of the neoplasm has not been observed 6 months after surgery.     

Social rank and sex ratio of captive long-tailed macaque females (Macaca fascicularis)

Variation in birth sex ratios in primates can be accounted for by two hypotheses: the local resource competition hypothesis [Silk: American Naturalist 121:56–66, 1983] and the hypothesis of Trivers & Willard [Science 179:90–92, 1973] concerning the maternal effect on the quality of a male. We examined the effects of female dominance rank on aspects of reproduction in three well-established captive groups of long-tailed macaques (Macaca fascicularis). High-ranking females produced a higher proportion of sons than low-ranking females, and factors other than rank did not have significant effects on birth sex ratios. Interbirth intervals following daughters were longer than those following sons, but they were independent of the mother's rank. The sons of high-ranking mothers had better survival prospects than sons of low-ranking mothers in some of the groups; no such difference was found for daughters. Overall, there was no sex difference in survival up to 5 years of age. These results support the Trivers-Willard hypothesis rather than the local resource competition hypothesis. An analysis of interbirth intervals suggested that the deviation in birth sex ratio is already established at conception.     

The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand

BACKGROUND: Long-tailed and rhesus macaques are widely used in biomedical research; therefore, the known blood group is important. METHODS: The human-type ABO blood group was determined in wild or semi-wild long-tailed and rhesus macaques in Thailand. A total of 729 long-tailed and 160 rhesus macaques from 20 localities were temporarily caught. RESULTS: The frequency profiles of blood groups, calculated by averaging the frequency of each troop in long-tailed and rhesus macaques, were AB > O > B > A at 29.6%, 27.4%, 27.2%, and 15.8%, and B > AB > A > O at 39.6%, 33.4%, 18.2%, and 8.8%, respectively. Irrespective of locality, the frequencies were AB > O > B > A of 29.6%, 28.0%, 24.4%, and 18.0%, and AB > B > A > O of 37.5%, 28.7%, 26.9%, and 6.9%, respectively, for all long-tailed and rhesus macaques. The frequency profile of blood groups in Thai rhesus macaques was somewhat similar to that in the parapatric long-tailed macaques; however, it was different from other rhesus populations where only group B was detected. CONCLUSIONS: Our data support the hypothesis that Indochinese rhesus macaques are hybrids between rhesus and long-tailed macaques in the past.     

Characterization of the rhesus macaque (Macaca mulatta) equivalent of HLA-F

Nucleotide sequence analysis of rhesus macaque major histocompatibility complex class I cDNAs allowed the identification of the orthologue of HLA-F, designated Mamu-F. Comparison of Mamu-F with earlier published human and chimpanzee orthologues demonstrated that these sequences share a high degree of similarity, both at the nucleotide and amino acid level, whereas a New World monkey (cotton-top tamarin) equivalent is more distantly related. Exon 7, encoding one of the cytoplasmatic domains, is absent for all primate Mhc-F cDNA sequences analyzed so far. In contrast to the human, chimpanzee, and rhesus macaque equivalents, the cotton-top tamarin Saoe-F gene seems to have accumulated far more nonsynomynous than synonymous differences.The nucleotide sequence data reported in this paper have been submitted to the Genbank nucleotide sequence database and have been assigned the accession number Z 21819.