Heterologous prime-boost immunization induces protection against dengue virus infection in cynomolgus macaques.

IMPORTANCE: Currently licensed dengue vaccines do not induce long-term protection in children without previous exposure to dengue viruses in nature. These vaccines are based on selected attenuated strains of the four dengue serotypes and employed in combination for two or three consecutive doses. In our search for a better dengue vaccine candidate, live attenuated strains were followed by non-infectious virus-like particles or the plasmids that generate these particles upon injection into the body. This heterologous prime-boost immunization induced elevated levels of virus-specific antibodies and helped to prevent dengue virus infection in a high proportion of vaccinated macaques. In macaques that remained susceptible to dengue virus, distinct mechanisms were found to account for the immunization failures, providing a better understanding of vaccine actions. Additional studies in humans in the future may help to establish whether this combination approach represents a more effective means of preventing dengue by vaccination.

Influence of COVID-19 on the emergence of stone-tool use behavior in a population of common long-tailed macaques (Macaca fascicularis fascicularis) in Thailand.

Stone tool use is a rare behavior across nonhuman primates. Here we report the first population of common long-tailed macaques (Macaca fascicularis fascicularis) who customarily used stone tools to open rock oysters (Saccostrea forskali) on a small island along the Thai Gulf in Koh Ped (KPE), eastern Thailand. We observed this population several times during the past 10 years, but no stone-tool use behavior was observed until our survey during the coronavirus disease 2019 (COVID-19) pandemic in July 2022. KPE is located in Pattaya City, a hotspot for tourism in Thailand. Tourists in this area frequently provided large amounts of food for the monkeys on KPE. During the COVID-19 curfew, however, tourists were not allowed to access the island, and monkeys began to face food scarcity. During this time, we observed stone-tool use behavior for the first time on KPE. Based on our observations, the first tool manipulation was similar to stone throwing (a known precursor of stone tool use). From our observations in March 2023, we found 17 subadult/adult animals performing the behavior, 15 of 17 were males and mostly solitary while performing the behavior. The M. f. fascicularis subspecies was confirmed by distribution, morphological characteristics, and mtDNA and SRY gene sequences. Taken together, we proposed that the stone tool use behavior in the KPE common long-tailed macaques emerged due to the COVID-19 food scarcity. Since traveling is no longer restricted many tourists have started coming back to the island, and there is a high risk for this stone tool-use behavior to disappear within this population of long-tailed macaques.

Prevalence of Mycobacterium tuberculosis Complex among Wild Rhesus Macaques and 2 Subspecies of Long-Tailed Macaques, Thailand, 2018-2022.

We identified tuberculosis in 1,836 macaques from 6 wild rhesus (Macaca mulatta), 23 common long-tailed (M. fascicularis fascicularis), and 6 Burmese long-tailed (M. fascicularis aurea) macaque populations in Thailand. We captured, anesthetized, and collected throat, buccal, and rectal swab specimens from the macaques. We screened swabs for Mycobacterium tuberculosis complex (MTBC) using insertion sequence 6110-specific nested PCR. We found higher MTBC prevalence at both population and individual levels among M. mulatta than M. fascicularis fascicularis macaques; all 3 M. fascicularis aurea macaque populations were positive for tuberculosis. We found that throat swab specimens provided the best sample medium for detecting MTBC. Our results showed no difference in MTBC prevalence between male and female animals, but a higher percentage of adults were infected than subadults and juveniles. Although we detected no association between frequency of human-macaque interaction and MTBC prevalence, bidirectional zoonotic transmission should be considered a possible public health concern.

Simulation and social network analysis provide insight into the acquisition of tool behaviour in hybrid macaques.

The pathways through which primates acquire skills are a central focus of cultural evolution studies. The roles of social and genetic inheritance processes in skill acquisition are often confounded by environmental factors. Hybrid macaques from Koram Island (Thailand) provide an opportunity to examine the roles of inheritance and social learning to skill acquisition within a single ecological setting. These hybrids are a cross between tool-using Burmese long-tailed (Macaca fascicularis aurea) and non-tool-using common long-tailed macaques (Macaca fascicularis fascicularis). This population provides an opportunity to explore the roles of social learning and inheritance processes while being able to exclude underlying ecological factors. Here, we investigate the roles of social learning and inheritance in tool use prevalence within this population using social network analysis and simulation. Agent-based modelling (ABM) is used to generate expectations for how social/asocial learning and inheritance structure the patterning in a social network. The results of the simulation show that various transmission mechanisms can be differentiated based on associations between individuals in a social network. The results provide an investigative framework for discussing tool use transmission pathways in the Koram social network. By combining ABM, network analysis, and behavioural data from the field we can investigate the roles social learning and inheritance play in tool acquisition of wild primates.

Precision spinal gene delivery-induced functional switch in nociceptive neurons reverses neuropathic pain.

Second-order spinal cord excitatory neurons play a key role in spinal processing and transmission of pain signals to the brain. Exogenously induced change in developmentally imprinted excitatory neurotransmitter phenotypes of these neurons to inhibitory has not yet been achieved. Here, we use a subpial dorsal horn-targeted delivery of AAV (adeno-associated virus) vector(s) encoding GABA (gamma-aminobutyric acid) synthesizing-releasing inhibitory machinery in mice with neuropathic pain. Treated animals showed a progressive and complete reversal of neuropathic pain (tactile and brush-evoked pain behavior) that persisted for a minimum of 2.5 months post-treatment. The mechanism of this treatment effect results from the switch of excitatory to preferential inhibitory neurotransmitter phenotype in dorsal horn nociceptive neurons and a resulting increase in inhibitory activity in regional spinal circuitry after peripheral nociceptive stimulation. No detectable side effects (e.g., sedation, motor weakness, loss of normal sensation) were seen between 2 and 13 months post-treatment in naive adult mice, pigs, and non-human primates. The use of this treatment approach may represent a potent and safe treatment modality in patients suffering from spinal cord or peripheral nerve injury-induced neuropathic pain.

Developmental and environmental modulation of fecal thyroid hormone levels in wild Assamese macaques (Macaca assamensis).

Thyroid hormones are key modulators of development, as well as mediators of environmental conditions, by regulating developmental processes and metabolism in primates. Hormone measurement in noninvasively collected samples, that is, feces and urine, is a valuable tool for studying the endocrine function of wildlife, and recent studies have demonstrated the feasibility of measuring thyroid hormones in fecal samples of zoo-housed and wild nonhuman primates. Our study aimed to (i) validate the measurement of immunoreactive fecal total triiodothyronine (IF-T3) in wild Assamese macaques (Macaca assamensis) and (ii) to investigate its developmental changes and its response to environmental changes, including stress responses, in immature individuals. Fecal samples and environmental parameters were collected from individuals of three social groups of wild Assamese macaques living at Phu Khieo Wildlife Sanctuary, Northeastern Thailand. Our study confirmed the methodological feasibility and biological validity of measuring IF-T3 in this population. Specifically, the biological validation demonstrated higher IF-T3 levels in immatures compared to adults, and higher levels in females during late gestation compared to the preconception stage. Our analysis of IF-T3 levels in developing immature macaques revealed a significant increase with age. Furthermore, we found a positive association between IF-T3 and immunoreactive fecal glucocorticoid levels, an indicator of the physiological stress response. Neither minimum temperature nor fruit abundance predicted variation in IF-T3 levels in the immatures. Our findings indicate the possibility for differing effects of climatic factors and food availability on thyroid hormone level changes in immature versus adult animals and in wild compared to experimental conditions. Overall, our study provides the basis for further investigations into the role of thyroid hormones in shaping species-specific traits, growth, and overall primate development.

Receptor binding domain proteins of SARS-CoV-2 variants produced in Nicotiana benthamiana elicit neutralizing antibodies against variants of concern.

The constantly emerging severe acute respiratory syndrome-coronavirus 2 (SARS-CoV-2) variants of concerns (VOCs) with mutations in the receptor-binding domain (RBD) spread rapidly and has become a severe public health problem worldwide. Effective vaccines and optimized booster vaccination strategies are thus highly required. Here, the gene encoding six different RBD (Alpha, Beta, Gamma, Kappa, Delta, and Epsilon variants) along with the Fc fragment of human IgG1 (RBD-Fc) was cloned into plant expression vector and produced in Nicotiana benthamiana by transient expression. Further, the immunogenicity of plant-produced variant RBD-Fc fusion proteins were tested in cynomolgus monkeys. Each group of cynomolgus monkeys was immunized three times intramuscularly with variant RBD-Fc vaccines at Day 0, 21, 42, and neutralizing antibody responses were evaluated against ancestral (Wuhan), Alpha, Beta, Gamma, and Delta variants. The results showed that three doses of the RBD-Fc vaccine significantly enhanced the immune response against all tested SARS-CoV-2 variants. In particular, the vaccines based on Delta and Epsilon mutant RBD elicit broadly neutralizing antibodies against ancestral (Wuhan), Alpha, and Delta SARS-CoV-2 variants whereas Beta and Gamma RBD-Fc vaccines elicit neutralizing antibodies against their respective SARS-CoV-2 strains. The Delta and Epsilon RBD-Fc based vaccines displayed cross-reactive immunogenicity and might be applied as a booster vaccine to induce broadly neutralizing antibodies. These proof-of-concept results will be helpful for the development of plant-derived RBD-Fc-based vaccines against SARS-CoV-2 and its variants.

Comparison of neuroprotective effects of dihydrotestosterone, 17ß-estradiol, and Pueraria mirifica herb extract on cognitive impairment in androgen deficient male rats.

This study investigated the neuroprotective effects of dihydrotestosterone (DHT), 17ß-estradiol (E2), and Pueraria mirifica herb extract (PME; an alternative source of natural estrogens) on the (i) learning and memory in androgen-deficient male rats, and on the hippocampus expression levels of (ii) mRNA of genes associated with synaptic transmission and structure, neurofibrillary tangles, and amyloid plaques, and (iii) total and phosphorylated tau proteins. The four-month-old male rats were sham-operated or orchidectomized (ODX). The ODX rats were divided into four groups, and orally treated for 2 months with either 1 mL/d of distilled water or 100 mg/kg/d of PME; or subcutaneously injected with 1 mg/kg/d of DHT or 80 µg/kg/d of E2. The impairment of spatial learning behavior and memory capacity in the ODX rats was prevented by DHT, E2, and PME. Recovery of the orchidectomy-induced deterioration of the synaptic plasticity in the hippocampus of rats was ranked as E2 ≥ PME > DHT. Both DHT and PME mitigated the increased Tau3 and Tau4 mRNA levels, and Tau-5 and P-Tau Ser396 protein levels more than E2 (DHT ≥ PME > E2). Only DHT tended to decrease App mRNA expression level. In conclusion, DHT showed a stronger efficacy for mitigation of the impaired spatial learning behavior and memory capacity in androgen-deficient male rats compared to E2 and PME, and their mechanisms of action are slightly different.

Gene flow from rhesus (Macaca mulatta) to cynomolgus macaques (M. fascicularis) and effects of introgressive hybridization on reproduction in two biomedically relevant non-human primate species.

BACKGROUND: We compared the reproductive patterns of wild Indochinese and Sundaic cynomolgus macaques (Mf) exhibiting different levels of genetic admixture with rhesus macaques (Mm). METHODS: Ten adult females from each Indochinese (WHM) and Sundaic (KN/KTK) Mf populations, which exhibited 50% and 15% of Mm autosomal SNPs, were selected as focal animals. Animals were observed for 12 months, and the frequencies of sexual proceptivity, attractivity and receptivity, number of newborns, and changes in sex skin were recorded. RESULTS: Both populations showed all three sexual behaviors throughout the year, but they were classified as moderately seasonal breeders because their 3-month birth counts were as high as ~50%. The fecundity of WHM was lower than the KN/KTK. Changes in sex skin of WHM were more prone to Mm's pattern than the KN/KTK. CONCLUSION: The introgressive gene flow from Mm to Mf does not affect Mf's sexual behaviors; however, it can impact fecundity and physiological (sex skin) changes.

Importance of Thai macaque bioresources for biological research and human health.

During the past century, macaque bioresources have provided remarkable scientific and biomedical discoveries related to the understanding of human physiology, neuroanatomy, reproduction, development, cognition, and pathology. Considerable progress has been made, and an urgent need has arisen to develop infrastructure and viable settings to meet the current global demand in research models during the so-called new normal after COVID-19 era. This review highlights the critical need for macaque bioresources and proposes the establishment of a designated primate research center to integrate research in primate laboratories for the rescue and rehabilitation of wild macaques. Key areas where macaque models have been and continue to be essential for advancing fundamental knowledge in biomedical and biological research are outlined. Detailed genetic studies on macaque bioresources of Thai origin can further facilitate the rapid pace of vaccine discovery.

Population Structure of Macaca fascicularis aurea, and their Genetic Relationships with M. f. fascicularis and M. mulatta Determined by 868 RADseq-Derived Autosomal SNPs-A consideration for biomedical research.

BACKGROUND: This study examined the population structure of Macaca fascicularis aurea and their genetic relationships with M. f. fascicularis and M. mulatta. METHODS: The study analyzed 868 RADseq-derived SNPs from samples representing the entire distribution range of M. f. aurea, including their inter- and intraspecific hybrid zones. RESULTS: The study supports a M. mulatta/Indochinese M. f. fascicularis, Sundaic M. f. fascicularis, and M. f. aurea trichotomy; M. f. aurea was genetically distinct from both forms of M. f. fascicularis and M. mulatta. Hybridization between M. f. aurea and M. f. fascicularis occurred in two directions: south-north (8°25' to 15°56') and west-east (98°28' to 99°02'). Low levels of M. mulatta introgression were also detected in M. f. aurea. CONCLUSION: This study showcases a complicated scenario of genetic relationships between the M. fascicularis subspecies and between M. fascicularis and M. mulatta and underscores the importance of these taxa's population structure and genetic relationships for biomedical research.

Comparative Pharmacokinetics of Puerarin Alone and in Pueraria mirifica Extract in Female Cynomolgus Monkeys.

Pueraria mirifica is an endemic Thai plant that has been used for rejuvenation and in the relief of various aging diseases. Puerarin is one of the major isoflavones found in this plant and shows several pharmacological activities in relation to the Thai traditional use of P. mirifica. Therefore, comparative pharmacokinetics of pure puerarin alone and that in a P. mirifica extract in cynomolgus monkeys were conducted in order to investigate the pharmacokinetic profiles of the 2 preparations. To this end, puerarin and P. mirifica extract, at an equivalent dose of 10 mg/kg of puerarin, were orally dosed to adult female monkeys for 7 consecutive days. A single intravenous injection of puerarin at a dose of 1 mg/kg was also peformed. Serial blood samples and excreta were collected from 0 - 24 h and 0 - 48 h after dosing. Determination of the puerarin levels and its metabolites in biological samples was conducted by liquid chromatography tandem mass spectrometry. Plasma levels of aspartate aminotransferase, alanine aminotransferase, and creatinine fluctuated in the normal range, with no abnormal physical signs in the animal. The absolute oral bioavailability of puerarin was approximately 1% in both preparations. Accumulation of puerarin was found after oral dosing for 7 consecutive days in both groups. Major metabolites of puerarin found in monkeys were hydroxylation and deglycosylation products. A negligible amount of unchanged puerarin was detected in urine and feces. Pharmacokinetic profiles obtained from this study could help to design the prescribed remedy of puerarin and P. mirifica extract phytopharmaceutical products for human use.

Oral-fecal mycobiome in wild and captive cynomolgus macaques (Macaca fascicularis).

Cynomolgus macaque (Macaca fascicularis) is currently a common animal model for biomedical research. The National Primate Research Center of Thailand, Chulalongkorn University (NPRCT-CU) translocated wild-borne macaques to reared colony for research purposes. At present, no studies focus on fungal microbiome (Mycobiome) of this macaque. The functional roles of mycobiome and fungal pathogens have not been elucidated. Thus, this study aimed to investigate and compare oral and fecal mycobiome between wild and captive macaques by using high-throughput sequencing on internal transcribed spacer 2 (ITS2) rDNA. The results showed that the mycobiome of wild macaque has greater alpha diversity. The fecal mycobiome has more limited alpha diversity than those in oral cavity. The community is mainly dominated by saprophytic yeast in Kasachstania genus which is related to aiding metabolic function in gut. The oral microbiome of most captive macaques presented the Cutaneotrichosporon suggesting the fungal transmission through skin-oral contact within the colony. The potential pathogens that would cause harmful transmission in reared colonies were not found in either group of macaques but the pathogen prevention and animal care is still important to be concerned. In conclusion, the results of gut mycobiome analysis in Thai cynomolgus macaques provide us with the basic information of oral and fecal fungi and for monitoring macaque's health status for animal care of research use.

Secondary contact and genomic admixture between rhesus and long-tailed macaques in the Indochina Peninsula.

Understanding the process and consequences of hybridization is one of the major challenges in evolutionary biology. A growing body of literature has reported evidence of ancient hybridization events or natural hybrid zones in primates, including humans; however, we still have relatively limited knowledge about the pattern and history of admixture because there have been little studies that simultaneously achieved genome-scale analysis and a geographically wide sampling of wild populations. Our study applied double-digest restriction site-associated DNA sequencing to samples from the six localities in and around the provisional hybrid zone of rhesus and long-tailed macaques and evaluated population structure, phylogenetic relationships, demographic history, and geographic clines of morphology and allele frequencies. A latitudinal gradient of genetic components was observed, highlighting the transition from rhesus (north) to long-tailed macaque distribution (south) as well as the presence of one northern population of long-tailed macaques exhibiting unique genetic structure. Interspecific gene flow was estimated to have recently occurred after an isolation period, and the migration rate from rhesus to long-tailed macaques was slightly greater than in the opposite direction. Although some rhesus macaque-biased alleles have widely introgressed into long-tailed macaque populations, the inflection points of allele frequencies have been observed as concentrated around the traditionally recognized interspecific boundary where morphology discontinuously changed; this pattern was more pronounced in the X chromosome than in autosomes. Thus, due to geographic separation before secondary contact, reproductive isolation could have evolved, contributing to the maintenance of an interspecific boundary and species-specific morphological characteristics.

The human-primate interface in the New Normal: Challenges and opportunities for primatologists in the COVID-19 era and beyond.

The emergence of SARS-CoV-2 in late 2019 and human responses to the resulting COVID-19 pandemic in early 2020 have rapidly changed many aspects of human behavior, including our interactions with wildlife. In this commentary, we identify challenges and opportunities at human-primate interfaces in light of COVID-19, focusing on examples from Asia, and make recommendations for researchers working with wild primates to reduce zoonosis risk and leverage research opportunities. First, we briefly review the evidence for zoonotic origins of SARS-CoV-2 and discuss risks of zoonosis at the human-primate interface. We then identify challenges that the pandemic has caused for primates, including reduced nutrition, increased intraspecific competition, and increased poaching risk, as well as challenges facing primatologists, including lost research opportunities. Subsequently, we highlight opportunities arising from pandemic-related lockdowns and public health messaging, including opportunities to reduce the intensity of problematic human-primate interfaces, opportunities to reduce the risk of zoonosis between humans and primates, opportunities to reduce legal and illegal trade in primates, new opportunities for research on human-primate interfaces, and opportunities for community education. Finally, we recommend specific actions that primatologists should take to reduce contact and aggression between humans and primates, to reduce demand for primates as pets, to reduce risks of zoonosis in the context of field research, and to improve understanding of human-primate interfaces. Reducing the risk of zoonosis and promoting the well-being of humans and primates at our interfaces will require substantial changes from "business as usual." We encourage primatologists to help lead the way.

Population genetics of the ABO locus within the rhesus (Macaca mulatta) and cynomolgus (M. fascicularis) macaque hybrid zone.

Knowledge of the macaque ABO blood group system has been critical in the development of nonhuman primates (NHPs) as a translational model. Serving not only as a useful homologue of the disease-linked ABO system in humans, macaque ABO blood groups must be typed in colonies prior to performing experimental procedures requiring blood transfusion or transplantation. While the rates of blood type incompatibility and the distributions of A, B and AB blood groups are known in large samples of rhesus (Macaca mulatta) and cynomolgus (M. fascicularis) macaques, there is a dearth of blood type data from macaque populations occupying the rhesus-cynomolgus hybrid zone in Southeast Asia. Using molecular phenotyping, we profiled ABO blood group distributions of 232 macaques from 10 populations in the hybrid zone and compared them to pure blood populations of the two species. We found that while these distributions are significantly different in most populations, there was a lack of differentiation between the hybrid and cynomolgus macaques as well as between the Thai and neighbouring populations. This supports a more expansive model of hybridization between rhesus and cynomolgus macaques than often proposed and highlights the increased need for consideration of population genetic structure in biomedical studies that employ macaques as animal models. Additionally, we report an enrichment of indeterminate blood types in the hybrid populations.

Locomotor Kinematics of Two Semi-Wild Macaque Species (Macaca assamensis and Macaca arctoides) in Thailand.

This project aimed to investigate primate locomotor kinematics noninvasively in the wild. Semi-wild Assamese and stump-tailed macaques were selected for the study, which was performed in Thailand. We investigated their locomotor kinematics and its relationship to habitat use. The macaques' positional behavior was recorded with two video cameras, and kinematic parameters were estimated during terrestrial quadrupedal locomotion, using the markerless method. The data analyzed so far revealed that stump-tailed macaques walk with longer, less frequent strides than Assamese macaques. Although stump-tailed macaques present a smaller angular excursion of the shoulder joint than Assamese macaques, they exhibited a relatively large shoulder girdle motion and anteroposterior translation of the shoulder, which increased their stride length. Additionally, stump-tailed macaques exhibited a digitigrade gait and elbow extension, suggesting a good adaptation to terrestrial locomotion. Assamese macaques, on the other hand, exhibited a gait that did not seem optimized for terrestrial locomotion, using the hands in a palmigrade posture and frequently flexing the fingers at varying degrees. The kinematic characteristics of the two species studied is consistent with previous field observations reporting that Assamese macaques are highly arboreal, whereas stump-tailed macaques are more terrestrial.

Young macaques (Macaca fascicularis) preferentially bias attention towards closer, older, and better tool users.

Examining how animals direct social learning during skill acquisition under natural conditions, generates data for examining hypotheses regarding how transmission biases influence cultural change in animal populations. We studied a population of macaques on Koram Island, Thailand, and examined model-based biases during interactions by unskilled individuals with tool-using group members. We first compared the prevalence of interactions (watching, obtaining food, object exploration) and proximity to tool users during interactions, in developing individuals (infants, juveniles) versus mature non-learners (adolescents, adults), to provide evidence that developing individuals are actively seeking information about tool use from social partners. All infants and juveniles, but only 49% of mature individuals carried out interacted with tool users. Macaques predominantly obtained food by scrounging or stealing, suggesting maximizing scrounging opportunities motivates interactions with tool users. However, while interactions by adults was limited to obtaining food, young macaques and particularly infants also watched tool users and explored objects, indicating additional interest in tool use itself. We then ran matrix correlations to identify interaction biases, and what attributes of tool users influenced these. Biases correlated with social affiliation, but macaques also preferentially targeted tool users that potentially increase scrounging and learning opportunities. Results suggest that social structure may constrain social learning, but the motivation to bias interactions towards tool users to maximize feeding opportunities may also socially modulate learning by facilitating close proximity to better tool users, and further interest in tool-use actions and materials, especially during development.

Whole Mitochondrial Genomic and Y-Chromosomal Phylogenies of Burmese Long-Tailed Macaque (Macaca fascicularis aurea) Suggest Ancient Hybridization between fascicularis and sinica Species Groups.

Macaca fascicularis aurea (Burmese long-tailed macaque) is 1 of the 10 subspecies of Macaca fascicularis. Despite having few morphological differences from other subspecies, a recent phylogeographic study showed that M. f. aurea is clearly distinct genetically from Macaca fascicularis fascicularis (common long-tailed macaque) and suggests that M. f. aurea experienced a disparate evolutionary pathway versus other subspecies. To construct a detailed evolutionary history of M. f. aurea and its relationships with other macaque species, we performed phylogenetic analyses and divergence time estimation of whole mitochondrial genomes (2 M. f. aurea, 8 M. f. fascicularis, and 16 animals of 12 macaque species) and 2871 bp of the Y chromosome (1 M. f. aurea, 2 M. f. fascicularis, and 5 animals of 5 macaque species) and haplotype network analysis of 758 bp of the Y chromosome (1 M. f. aurea, 2 M. f. fascicularis, and 21 animals of 19 macaque species). Whereas the Y chromosome of M. f. aurea clustered with those of the fascicularis species group in the phylogenetic and haplotype network analyses, its mtDNA clustered within the clade of the sinica species group. Based on this phylogenetic incongruence and the estimated divergence times, we propose that proto-M. f. aurea underwent hybridization with a population of the sinica species group between 2.5 and 0.95 MYA after divergence from the common ancestor of M. fascicularis. Hybridization and introgression might have been central in the evolution of M. f. aurea, similar to what occurred in the evolution of other macaque species and subspecies.

Short dispersal distance of males in a wild white-handed gibbon (Hylobates lar) population.

OBJECTIVES: It has long been recognized that in gibbons both sexes disperse from the natal group. However, the fate of dispersed individuals was rarely documented. Here we provide the first detailed information on sex differences in dispersal patterns by analyzing the spatial genetic structure of a well-known white-handed gibbon (Hylobates lar) population. MATERIALS AND METHODS: Mitochondrial DNA (mtDNA) and Y-chromosomal haplotypes, and autosomal microsatellite genotypes were determined for individuals of the Mo Singto study site, Khao Yai National Park, Thailand. Mantel tests for the three genetic marker types were performed for 17 gibbon groups comprising 23 adult males and 18 adult females. RESULTS: Significant positive Mantel correlations were observed for spatial distance and both autosomal microsatellite-based as well as Y-chromosomal haplotype-based genetic distance among adult males. Neighboring adult males tended to be genetically related and share Y-chromosomal haplotypes. Conversely, no significant Mantel correlations were observed either in autosomal microsatellites or mtDNA among adult females. DISCUSSION: Our results confirm, at a genetic level, hypotheses from long-term demographic observations that white-handed gibbon males of the Mo Singto population primarily disperse into adjacent groups. Instead, females disperse more opportunistically either to adjacent or more distant groups. This sex-specific difference reflects an apparent greater tolerance between males than between females. The higher tolerance of adult males allows the formation of stable multimale groups and facilitates male dispersal into an adjacent group. Stable multifemale groups have never been documented for white-handed gibbons probably due to feeding competition between females.