Mimetic muscles in a despotic macaque (Macaca mulatta) differ from those in a closely related tolerant macaque (M. nigra)

Facial displays (or expressions) are a primary means of visual communication among conspecifics in many mammalian orders. Macaques are an ideal model among primates for investigating the co‐evolution of facial musculature, facial displays, and social group size/behavior under the umbrella of “ecomorphology”. While all macaque species share some social behaviors, dietary, and ecological parameters, they display a range of social dominance styles from despotic to tolerant. A previous study found a larger repertoire of facial displays in tolerant macaque species relative to despotic species. The present study was designed to further explore this finding by comparing the gross morphological features of mimetic muscles between the Sulawesi macaque (Macaca nigra), a tolerant species, and the rhesus macaque (M. mulatta), a despotic species. Five adult M. nigra heads were dissected and mimetic musculature was compared to those from M. mulatta. Results showed that there was general similarity in muscle presence/absence between the species as well as muscle form except for musculature around the external ear. M. mulatta had more musculature around the external ear than M. nigra. In addition, M. nigra lacked a zygomaticus minor while M. mulatta is reported to have one. These morphological differences match behavioral observations documenting a limited range of ear movements used by M. nigra during facial displays. Future studies focusing on a wider phylogenetic range of macaques with varying dominance styles may further elucidate the roles of phylogeny, ecology, and social variables in the evolution of mimetic muscles within Macaca

A genetic comparison of two alleged subspecies of P hilippine cynomolgus macaques

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 . Am J Phys Anthropol 155:136–148, 2014. © 2014 Wiley Periodicals, Inc.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/108326/1/ajpa22564.pd

Opsin genes of select treeshrews resolve ancestral character states within Scandentia

Treeshrews are small, squirrel-like mammals in the order Scandentia, which is nested together with Primates andDermoptera in the superordinal group Euarchonta. They are often described as living fossils, and researchers havelong turned to treeshrews as a model or ecological analogue for ancestral primates. A comparative study of colourvision-encoding genes within Scandentia found a derived amino acid substitution in the long-wavelength sensitiveopsin gene (OPN1LW) of the Bornean smooth-tailed treeshrew (Dendrogale melanura). The opsin, by inference, isred-shifted by ca. 6 nm with an inferred peak sensitivity of 561 nm. It is tempting to view this trait as a novel visualadaptation; however, the genetic and functional diversity of visual pigments in treeshrews is unresolved outside ofBorneo. Here we report gene sequences from the northern smooth-tailed treeshrew (Dendrogale murina) and theMindanao treeshrew (Tupaia everetti, the senior synonym of Urogale everetti). We found that the opsin genes areunder purifying selection and that D. murina shares the same substitution as its congener, a result that distinguishesDendrogale from other treeshrews, including T. everetti. We discuss the implications of opsin functional variation inlight of limited knowledge about the visual ecology of smooth-tailed treeshrews

Social tolerance in wild female crested macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia.

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared-teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared-teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females' social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems

Highly polymorphic microsatellite markers for the assessment of male reproductive skew and genetic variation in Critically Endangered crested macaques (Macaca nigra)

Genetic analyses based on non-invasively collected samples have become an important tool for evolutionary biology and conservation. Crested macaques (Macaca nigra), endemic to Sulawesi, Indonesia, are important for our understanding of primate evolution as Sulawesi macaques represent an exceptional example of primate adaptive radiation. Crested macaques are also Critically Endangered. However, to date we know very little about their genetics. The aim of our study was to find and validate microsatellite markers useful for evolutionary, conservation and other genetic studies on wild crested macaques. Using faecal samples of 176 wild macaques living in the Tangkoko Reserve, Sulawesi, we identified 12 polymorphic microsatellite loci through cross-species PCR amplification with later modification of some of these primers. We tested their suitability by investigating and exploring patterns of paternity, observed heterozygosity and evidence for inbreeding. We assigned paternity to 63 of 65 infants with high confidence. Among cases with solved paternity, we found no evidence of extra-group paternity and natal breeding. We found a relatively steep male reproductive skew B index of 0.330±0.267; mean±SD) and mean alpha paternity of 65% per year with large variation across groups and years (29-100%). Finally, we detected an excess in observed heterozygosity and no evidence of inbreeding across our three study groups, with an observed heterozygosity of 0.766±0.059 and expected heterozygosity of 0.708±0.059, and an inbreeding coefficient of -0.082±0.035. Our results indicate that the selected markers are useful for genetic studies on wild crested macaques, and possible also other Sulawesi and closely related macaques. They further suggest that the Tangkoko population of crested macaques is still genetically variable despite its small size, isolation and the species’ reproductive patterns. This gives us hope that other endangered primate species living in small, isolated populations may also retain a healthy gene pool, at least in the short term

Rates of human–macaque interactions affect grooming behavior among urban‐dwelling rhesus macaques (Macaca mulatta)

OBJECTIVES: The impact of anthropogenic environmental changes may impose strong pressures on the behavioral flexibility of free-ranging animals. Here, we examine whether rates of interactions with humans had both a direct and indirect influence on the duration and distribution of social grooming in commensal rhesus macaques (Macaca mulatta). MATERIALS AND METHODS: Data were collected in two locations in the city of Shimla in northern India: an urban setting and a temple area. We divided these two locations in a series of similar-sized physical blocks (N = 48) with varying rates of human-macaque interactions. We conducted focal observations on three free-ranging rhesus macaque groups, one in the urban area and two in the temple area. RESULTS: Our analysis shows that macaques engaged in shorter grooming bouts and were more vigilant while grooming in focal sessions during which they interacted with people more frequently, suggesting that humans directly affected grooming effort and vigilance behavior. Furthermore, we found that in blocks characterized by higher rates of human-macaque interactions grooming bouts were shorter, more frequently interrupted by vigilance behavior, and were less frequently reciprocated. DISCUSSION: Our work shows that the rates of human-macaque interaction had both a direct and indirect impact on grooming behavior and that macaques flexibly modified their grooming interactions in relation to the rates of human-macaque interaction to which they were exposed. Because grooming has important social and hygienic functions in nonhuman primates, our work suggests that human presence can have important implications for animal health, social relationships and, ultimately, fitness. Our results point to the need of areas away from people even for highly adaptable species where they can engage in social interactions without human disruption.National Science Foundatio

Plasmodium knowlesi transmission:integrating quantitative approaches from epidemiology and ecology to understand malaria as a zoonosis

The public health threat posed by zoonotic Plasmodium knowlesi appears to be growing: it is increasingly reported across South East Asia, and is the leading cause of malaria in Malaysian Borneo. Plasmodium knowlesi threatens progress towards malaria elimination as aspects of its transmission, such as spillover from wildlife reservoirs and reliance on outdoor-biting vectors, may limit the effectiveness of conventional methods of malaria control. The development of new quantitative approaches that address the ecological complexity of P. knowlesi, particularly through a focus on its primary reservoir hosts, will be required to control it. Here, we review what is known about P. knowlesi transmission, identify key knowledge gaps in the context of current approaches to transmission modelling, and discuss the integration of these approaches with clinical parasitology and geostatistical analysis. We highlight the need to incorporate the influences of fine-scale spatial variation, rapid changes to the landscape, and reservoir population and transmission dynamics. The proposed integrated approach would address the unique challenges posed by malaria as a zoonosis, aid the identification of transmission hotspots, provide insight into the mechanistic links between incidence and land use change and support the design of appropriate interventions

Genetic variation and evolution in the red cell carbonic anhydrase isozymes of macaque monkeys

The electrophoretic phenotypes of the two isozymes of red cell carbonic anhydrase, CA I and CA II, are described in nine species of macaque monkeys from southeast Asia and Japan. Twelve phenotypes of CA I, apparently under the control of seven alleles, and five phenotypes of CA II, under the control of three alleles, were found in the different macaque populations studied. Extensive electrophoretic polymorphisms of CA I were found in three species (Macaca nemestrina, Macaca speciosa , and Macaca fuscata) , and polymorphisms at the CA II locus were found in Macaca irus, Macaca mulatta , and M. nemestrina . In addition to the electrophoretic polymorphisms at the CA I locus in M. nemestrina , an inherited deficiency of CA I was also discovered in which approximately 30% of the individuals in all populations of M. nemestrina tested showed the deficient phenotype. Although the recessive gene controlling this deficiency appears to be an allele of the CA I locus, it is postulated that the CA I deficiency could also be under the control of a closely linked gene. The comparative data on the extent of genetic variation observed in the two isozymes of red cell carbonic anhydrase in macaques appear to support the concept that CA I has evolved more rapidly than CA II in mammals.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/44171/1/10528_2004_Article_BF00485644.pd

Transmission and control of Plasmodium knowlesi: a mathematical modelling study.

INTRODUCTION: Plasmodium knowlesi is now recognised as a leading cause of malaria in Malaysia. As humans come into increasing contact with the reservoir host (long-tailed macaques) as a consequence of deforestation, assessing the potential for a shift from zoonotic to sustained P. knowlesi transmission between humans is critical. METHODS: A multi-host, multi-site transmission model was developed, taking into account the three areas (forest, farm, and village) where transmission is thought to occur. Latin hypercube sampling of model parameters was used to identify parameter sets consistent with possible prevalence in macaques and humans inferred from observed data. We then explore the consequences of increasing human-macaque contact in the farm, the likely impact of rapid treatment, and the use of long-lasting insecticide-treated nets (LLINs) in preventing wider spread of this emerging infection. RESULTS: Identified model parameters were consistent with transmission being sustained by the macaques with spill over infections into the human population and with high overall basic reproduction numbers (up to 2267). The extent to which macaques forage in the farms had a non-linear relationship with human infection prevalence, the highest prevalence occurring when macaques forage in the farms but return frequently to the forest where they experience higher contact with vectors and hence sustain transmission. Only one of 1,046 parameter sets was consistent with sustained human-to-human transmission in the absence of macaques, although with a low human reproduction number (R(0H) = 1.04). Simulations showed LLINs and rapid treatment provide personal protection to humans with maximal estimated reductions in human prevalence of 42% and 95%, respectively. CONCLUSION: This model simulates conditions where P. knowlesi transmission may occur and the potential impact of control measures. Predictions suggest that conventional control measures are sufficient at reducing the risk of infection in humans, but they must be actively implemented if P. knowlesi is to be controlled

Population Recovery of Nicobar Long-Tailed Macaque Macaca fascicularis umbrosus following a Tsunami in the Nicobar Islands, India

Natural disasters pose a threat to isolated populations of species with restricted distributions, especially those inhabiting islands. The Nicobar long tailed macaque.Macaca fascicularis umbrosus, is one such species found in the three southernmost islands (viz. Great Nicobar, Little Nicobar and Katchal) of the Andaman and Nicobar archipelago, India. These islands were hit by a massive tsunami (Indian Ocean tsunami, 26 December 2004) after a 9.2 magnitude earthquake. Earlier studies [Umapathy et al. 2003; Sivakumar, 2004] reported a sharp decline in the population of M. f. umbrosus after thetsunami. We studied the distribution and population status of M. f. umbrosus on thethree Nicobar Islands and compared our results with those of the previous studies. We carried out trail surveys on existing paths and trails on three islands to get encounter rate as measure of abundance. We also checked the degree of inundation due to tsunami by using Normalized Difference Water Index (NDWI) on landsat imageries of the study area before and after tsunami. Theencounter rate of groups per kilometre of M. f. umbrosus in Great Nicobar, Little Nicobar and Katchal was 0.30, 0.35 and 0.48 respectively with the mean group size of 39 in Great Nicobar and 43 in Katchal following the tsunami. This was higher than that reported in the two earlier studies conducted before and after the tsunami. Post tsunami, there was a significant change in the proportion of adult males, adult females and immatures, but mean group size did not differ as compared to pre tsunami. The results show that population has recovered from a drastic decline caused by tsunami, but it cannot be ascertained whether it has reached stability because of the altered group structure. This study demonstrates the effect of natural disasters on island occurring species