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PubMed2006

Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups.

Humans are responsible for massive changes to primate habitats, and one unanticipated consequence of these alterations may be changes in host-parasite interactions. Edges are a ubiquitous aspect of human disturbance to forest landscapes. Here we examine how changes associated with the creation of edges in Kibale National Park, Uganda, alter the parasite community that is supported by two species of African colobines: the endangered red colobus (Piliocolobus tephrosceles) and the black-and-white colobus (Colobus guereza). An analysis of 822 fecal samples from edge and forest interior groups revealed no difference in the richness of parasite communities (i.e., the number of parasite species recovered from the host's fecal sample). However, for both species the proportion of individuals with multiple infections was greater in edge than forest interior groups. The prevalence of specific parasites also varied between edge and forest interior groups. Oesophagostomum sp., a potentially deleterious parasite, was 7.4 times more prevalent in red colobus on the edge than in those in the forest interior, and Entamoeba coli was four times more prevalent in red colobus on the edge than in animals from the forest interior. Environmental contamination with parasites (measured as parasite eggs/gm feces) by red colobus from the edge and forest interior differed in a similar fashion to prevalence for red colobus, but it did not differ for black-and-white colobus. For example, egg counts of Oesophagostomum sp. were 10 times higher in red colobus from the edge than in those from the interior. The less severe infections in the black-and-white colobus relative to the red colobus may reflect the fact that black-and-white colobus raid agricultural crops while red colobus do not. This nutritional gain may facilitate a more effective immune response to parasites by the black-and-white colobus. The fact that animals on the edge are likely not nutritionally stressed raises an intriguing question as to what facilitates the elevated infections in edge animals. We speculate that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human-health planning.

Animals↗
PubMed2006

Birth seasonality and interbirth interval of captive Rhinopithecus bieti.

This study, which is based on 10 years of birth records, shows that black-and-white snub-nosed monkeys (Rhinopithecus bieti) in captivity display marked birth seasonality. The birth season starts in December and ends in June, with a peak from March to May, and a median birth date of April 10. More male infants than female ones are born in captivity. More males were born at the Kunming Institute of Zoology (KIZ) than at the Kunming Zoo (KZ). Of 17 interbirth intervals (IBIs), 29% were from females that had lost an infant at <1 year of age or experienced stillbirth, and 71% were from females whose infant survived more than 1 year. The mean IBI for the former group (428+/-SD 87 days) was significantly shorter than that for the latter group (706+/-71 days), in agreement with reports of other Colobine species. Infant mortality was lower in captivity than in the field, which may reflect the relatively stable food availability and climate in captivity compared to the harsh conditions in the wild.

Animals↗
PubMed2006

What Hanuman langur males know about female reproductive status.

In species with a high risk of infanticide, a conflict of interest exists between the sexes over the amount of paternity information that is available to males. While females are expected to keep males unaware of their reproductive status in order to confuse paternity, selection should favor those male traits that enhance the males' assessment of female status and consequently of paternity probability. In Hanuman langurs (Semnopithecus entellus), a species that is extremely vulnerable to infanticide, females have been shown to successfully conceal the exact timing of ovulation from males--perhaps because they exhibit no sexual swelling and mate during all reproductive phases, including gestation. Nevertheless, it remains unclear whether males have hitherto unrecognized information about females' reproductive condition on a broader level that could still enhance male reproductive success. We investigated male assessment of female reproductive states in a population of wild Hanuman langurs as indicated by changes in male behavior, such as rates of copulations, anogenital inspections, and consortships, in relation to different female receptive periods (pregnant, fertile-nonconceptional, and conceptional). Our data indicate that males were able to discern qualitatively distinct reproductive states. Males were more interested in fertile than pregnant females, as indicated by higher copulation rates. Based on consortships, males distinguished fertile from nonfertile phases, as well as fertile, nonconceptional receptive periods from conceptional ones. Hanuman langur males are thus not as unaware of female reproductive condition as previously thought, supporting the idea of an ongoing battle of the sexes over paternity information. However, granting some knowledge while at the same time concealing the exact day of ovulation may also reflect a pure female strategy of balancing paternity concentration with paternity confusion, which is the most likely strategy in this system with high infanticide risk and male defense of infants.

Animals↗
PubMed2006

Mating behaviors of the proboscis monkey (Nasalis larvatus).

The mating behaviors of the proboscis monkey were observed in a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia, for a period of 30 months. Solicitation for copulation was initiated frequently by males and occasionally by females. Most copulations involved only one mount; however, some multiple-mount copulations were observed and a maximum of six mounts per copulation were recorded. The mean duration of mounts was about 27 sec. Nonsexual mounts (female-female, female-juvenile/infant, juvenile-juvenile, and juvenile-infant) were also observed. Female-female mounts occurred shortly after failed solicitations toward males were observed. Harassment by juveniles and/or infants was observed during copulation; however, these harassments apparently did not interfere with copulation. Sexual swelling was evident in 77.4% of copulating females, with copulating subadult females showing the most distinct swelling.

Animals↗
PubMed2004

Molar size and shape variations among Asian colobines.

Despite decades of research, little is known about morphometric differences within the dentition of Asian colobines. Although some differences, such as the M3 hypoconulid, are often cited as distinct among genera, no comprehensive assessment has been made. The objectives of this study were to document size and shape differences in third molars in eight Asian colobine genera, including Kasi, Nasalis, Presbytis, Pygathrix, Rhinopithecus, Semnopithecus, Simias, and Trachypithecus, and to quantify length differences for all molars in order to understand the potential impact of an occlusal surface area that includes the hypoconulid. To achieve these objectives, the most extensive survey yet published of Asian colobine dentition was conducted. Differences within and among genera for continuous and categorical variables were analyzed using descriptive statistics, chi-square, t-tests, and post hoc comparisons. Results indicate that species of Presbytis differ from all other Asian colobines in both the size and shape of the maxillary and mandibular third molars. Specifically, M3 of Presbytis is relatively shorter in length and less likely to exhibit a hypoconulid optimally positioned for occlusion with M3. Moreover, Presbytis expresses concomitant changes in the maxillary third molar such as absence of a distal shelf and/or a distal cusp with separated crests. We conclude that shape and size changes impact the molar size sequence patterns of Presbytis, setting this genus apart from all other Asian colobine taxa. These differences may reflect variation in overall body size, dietary adaptation, and phylogeny.

Animals↗
PubMed2005

Learning the ropes: The ontogeny of locomotion in red-shanked douc (Pygathrix nemaeus), Delacour's (Trachypithecus delacouri), and Hatinh langurs (Trachypithecus hatinhensis) I. positional behavior.

Recent studies at the Endangered Primate Rescue Center (EPRC) in the Socialist Republic of Vietnam's Cuc Phuong National Park by Byron et al. ([2002] Am. J. Phys. Anthropol. [Suppl.] 34:51) and Covert and Byron ([2002] Caring for Primates) revealed unexpected locomotor and postural behaviors in the red-shanked douc langur (Pygathrix nemaeus). This paper further elucidates the question of red-shanked douc suspensory behavior, and provides initial positional behavior data for two other rare Asian colobines, by comparing the ontogenetic positional behavior of red-shanked douc langurs, Delacour's langurs (Trachypithecus delacouri), and Hatinh langurs (Trachypithecus hatinhensis) at the EPRC. Two hundred and seven hours of positional behavior data were collected, with approximately equal amounts of data on each species, and equal amounts on adults and those less than 18 months in age. All young animals were more active than adults, used a wider repertoire of locomotor behaviors, and expressed suspensory behaviors more frequently than did the adults. Young animals also "invented" one new locomotor and two new postural behaviors. These differences are due to both play and explorative behavior, as well as to the youths' changing musculoskeletal systems. The number of positional behaviors utilized by the adults of these species is quite similar to one another (23-32), as is that utilized by the young (51-56). Douc langurs in both age categories used suspensory behaviors more frequently than did Delacour's and Hatinh langurs. Because the uniformity of enclosures offers a control, the results of this study generate hypotheses regarding adaptive radiations and niche partitioning in wild populations.

Animals↗
PubMed2003

The effect of forest clear-cutting on habitat use in Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia Nature Reserve, China.

The habitat use of two groups of Sichuan snub-nosed monkey ( Rhinopithecus roxellana) was observed, using the focal group method, for 7 months in four seasons from June 2000 to October 2001. The habitats were classed into primary forest and three successional habitats: after clear-cutting: grassland, shrub forest and young forest. The results showed that the large group of monkeys had larger range areas than the small group in the same season. Both groups had larger range sizes in summer or autumn than in winter or spring. They spent most of their time using primary forest and young forest, rarely used shrub forest and did not use grassland. In each season, they used the habitats non-randomly and preferred primary forest. The preference order of habitats for both groups every season was the same: primary forest > young forest > shrub forest >/= grassland. The results suggested that primary forest was high-quality habitat and should be conserved as a top priority. Clear-cutting would cause habitat loss and habitat fragmentation, and should therefore be prohibited. High-quality habitat for the monkeys is difficult to restore from clear-cutting.

Animal Migration↗
PubMed2004

Conflict and postconflict behaviour in captive black-and-white snub-nosed monkeys (Rhinopithecus bieti).

Black-and-white snub-nosed monkeys (Rhinopithecus bieti) have almost never been the subject of any behavioural observations in captivity. This study was aimed at providing preliminary information about agonistic and reconciliation behaviour in a group kept at the Kunming Institute of Zoology in China. Established procedures were used for this investigation (i.e., the postconflict/matched-control method and the time-rule method). Intra-group aggression rates were quite low. Postconflict affiliation as well as selective attraction of former opponents to each other following conflicts was demonstrated. Former opponents contacted each other earlier in postconflict periods than in matched-control periods. The average conciliatory tendency of all focal individuals combined was 54.5%. After an agonistic interaction, the first affiliative contact between former aggressors usually took place within the first minute. The behaviours most often shown as first affiliations after a conflict were body contact, mount, touch, and "hold-lumbar", of which the latter is an explicit reconciliatory gesture. Furthermore, the adult male intervened non-aggressively in 84% of all conflicts (n=25) among the adult females. Overall, the patterns of aggression and reconciliation observed in R. bieti bear many of the traits that characterise tolerant primate species.

Aggression↗
PubMed2006

Female transfer between one-male groups of proboscis monkey (Nasalis larvatus).

Successful or unsuccessful female transfers were observed seven times during a 32-month field study of proboscis monkeys (Nasalis larvatus) inhabiting a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia. In all cases, the females voluntarily left their own groups and immediately joined with another one. When adult females tried to shift to other groups, adult males called them back to their own groups, but appeared to be indifferent to subadult females. When the adult females returned, the males never attacked the females physically, but instead often emitted herding sounds to them. One subadult female was repelled by a resident adult female. When one adult female transferred into a new one-male group, she left her behind son in an all-male group. The number of females often fluctuated in most study groups, with this fluctuation being more prominent among subadult females than adult females. It is likely that female transfer in proboscis monkeys is not a rare occurrence and that it is especially common among sub-adult females.

Age Factors↗
PubMed2006

Social organization of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, Central China.

Sichuan snub-nosed monkeys were observed for 197 days from 2000 to 2003 in the Qinling Mountains, Central China. The study group was provisioned in 2001 allowing detailed observations of social organization based on individual identification. The group was composed of 45-82 monkeys, all of which belonged to one of 6-8 one-male units (OMU) that foraged to form one big group. The average unit size was 9.0+/-2.3, 8+/-1.5 in the winter and 11.1+/-2.0 in the spring. Immigration or emigration of one-male units to or from the foraging group was observed, as was migration of individuals in and out of OMU, especially for by subadult females and juveniles. Group size therefore tended to fluctuate with the number of OMU and the number of young monkeys present in the group. The OMU in the study area were smaller than those in Shennongjia area. The factors influencing the size of these OMU and the entire group are discussed.

Age Distribution↗
PubMed2006

Mitochondrial data support an odd-nosed colobine clade.

To obtain a more complete understanding of the evolutionary history of the leaf-eating monkeys we have examined the mitochondrial genome sequence of two African and six Asian colobines. Although taxonomists have proposed grouping the "odd-nosed" colobines (proboscis monkey, douc langur, and the snub-nosed monkey) together, phylogenetic support for such a clade has not been tested using molecular data. Phylogenetic analyses using parsimony, maximum likelihood, and Bayesian methods support a monophyletic clade of odd-nosed colobines consisting of Nasalis, Pygathrix, and Rhinopithecus, with tentative support for Nasalis occupying a basal position within this clade. The African and Asian colobine lineages are inferred to have diverged by 10.8 million years ago (mya or Ma). Within the Asian colobines the odd-nosed clade began to diversify by 6.7 Ma. These results augment our understanding of colobine evolution, particularly the nature and timing of the colobine expansion into Asia. This phylogenetic information will aid those developing conservation strategies for these highly endangered, diverse, and unique primates.

Animals↗
PubMed2003

Pseudogenization of the tumor-growth promoter angiogenin in a leaf-eating monkey.

Physiological functions of human genes may be studied by gene-knockout experiments in model organisms such as the mouse. This strategy relies on the existence of one-to-one gene orthology between the human and mouse. When lineage-specific gene duplication occurs and paralogous genes share a certain degree of functional redundancy, knockout mice may not provide accurate functional information on human genes. Angiogenin is a small protein that stimulates blood-vessel growth and promotes tumor development. Humans and related primates only have one angiogenin gene, while mice have three paralogous genes. This makes it difficult to generate angiogenin-knockout mice and even more difficult to interpret the genotype-phenotype relation from such animals should they be generated. We here show that in the douc langur (Pygathrix nemaeus), an Asian leaf-eating colobine monkey, the single-copy angiogenin gene has a one-nucleotide deletion in the sixth codon of the mature peptide, generating a premature stop codon. This nucleotide deletion is found in five unrelated individuals sequenced, and therefore is likely to have been fixed in the species. Five colobine species that are closely related to the douc langur have intact angiogenin genes, suggesting that the pseudogenization event was recent and unique to the douc langur lineage. This natural knockout experiment suggests that primate angiogenin is dispensable even in the wild. Further physiological studies of douc langurs may offer additional information on the role of this cancer-related gene in normal physiology of primates, including humans. Our findings also provide a strong case for the importance of evolutionary analysis in biomedical studies of gene functions.

Amino Acid Sequence↗
PubMed1996

A quick, direct method that can differentiate expressed mitochondrial genes from their nuclear pseudogenes.

Direct sequencing of mitochondrial DNA (mtDNA) following amplification using the polymerase chain reaction (PCR) has found widespread use in population genetic and phylogenetic research over the past few years. Recently, nuclear copies of mitochondrial genes have been reported in diverse eukaryotic species, often confounding such research (reviewed in [2,3]). Under certain circumstances, nuclear pseudogenes can be amplified more efficiently than the intended mtDNA target, even when using as template mtDNA that has been purified by gradient centrifugation. If the transfer of the gene copy to the nucleus happened recently, it can be difficult-if not impossible-to identify the legitimate mitochondrial sequence. Here, we present a simple method that can identify expressed mitochondrial genes, using the cytochrome b gene of the particularly problematical proboscis monkey as an example. Because mtDNA is transcribed and processed into polyadenylated mRNAs reverse transcription coupled to PCR can be used to amplify the expressed mitochondrial version. This method produced an unambiguous sequence for the proboscis monkey mitochondrial cytochrome b gene; in contrast, traditional DNA-based PCR methods produced ambiguous sequence, because many nuclear pseudogenes were present. Phylogenetic analysis of the cytochrome b gene suggests that the proboscis monkey groups with the Asian langurs, rather than forming a sister taxon to all Asian and African colobines as was previously suggested. Reverse transcriptase-coupled PCR should be applicable to many other cases of nuclear transfer of mtDNA, including those involving ribosomal genes.

Animals↗
PubMed1998

Mapping chromosomal homologies between humans and two langurs (Semnopithecus francoisi and S. phayrei) by chromosome painting.

Chromosomal homologies were established between human and two Chinese langurs (Semnopithecus francoisi, 2n = 44, and S. phayrei, 2n = 44) by chromosome painting with chromosome-specific DNA probes of all human chromosomes except the Y. Both langur species showed identical hybridization patterns in addition to similar G-banding patterns. In total, 23 human chromosome-specific probes detected 30 homologous chromosome segments in a haploid langur genome. Except for human chromosomes 1, 2, 6, 16 and 19 probes, which each gave signals on two non-homologous langur chromosomes respectively, all other probes each hybridized to a single chromosome. The results indicate a high degree of conservation of chromosomal synteny between human and these two Chinese langurs. The human chromosome 2 probe painted the entire euchromatic regions of langur chromosomes 14 and 19. Human chromosome 1 probe hybridized to three regions on langur autosomes, one region on langur chromosome 4 and two regions on langur chromosome 5. Human 19 probe hybridized on the same pattern to one region on chromosome 4 and to two regions on langur chromosome 5, where it alternated with the human chromosome 1 probe. Human 6 and 16 probes both hybridized to one region on each of the two langur autosomes 15 and 18. Only two langur chromosomes (12 and 21) were each labelled by probes specific for two whole human chromosomes (14 and 15 and 21 and 22 respectively). Comparison of the hybridization patterns of human painting probes on these two langurs with the data on other Old World primates suggests that reciprocal and Robertsonian translocations as will as inversions could have occurred since the divergence of human and the langurs from a common ancestor. This comparison also indicates that Asian colobines are karyotypically more closely related to each other that to African colobines.

Animals↗
PubMed2004

Construction, characterization and chromosomal mapping of bacterial artificial chromosome (BAC) library of Yunnan snub-nosed monkey (Rhinopithecus bieti).

We constructed a high redundancy bacterial artificial chromosome library of a seriously endangered Old World Monkey, the Yunnan snub-nosed monkey (Rhinopithecus bieti) from China. This library contains a total of 136 320 BAC clones. The average insert size of BAC clones was estimated to be 148 kb. The percentage of small inserts (50-100 kb) is 2.74%, and only 2.67% non-recombinant clones were observed. Assuming a similar genome size with closely related primate species, the Yunnan snub-nosed monkey BAC library has at least six times the genome coverage. By end sequencing of randomly selected BAC clones, we generated 201 sequence tags for the library. A total of 139 end-sequenced BAC clones were mapped onto the chromosomes of Yunnan snub-nosed monkey by fluorescence in-situ hybridization, demonstrating a high degree of synteny conservation between humans and Yunnan snub-nosed monkeys. Blast search against human genome showed a good correlation between the number of hit clones and the size of the chromosomes, an indication of unbiased chromosomal distribution of the BAC library. This library and the mapped BAC clones will serve as a valuable resource in comparative genomics studies and large-scale genome sequencing of nonhuman primates. The DNA sequence data reported in this paper were deposited in GenBank and assigned the accession number CG891489-CG891703.

Animals↗
PubMed1997

Episodic adaptive evolution of primate lysozymes.

Although the darwinian concept of adaptation was established nearly a century ago, it has been difficult to demonstrate rigorously that the amino-acid differences between homologous proteins from different species have adaptive significance. There are currently two major types of sequence tests for positive darwinian selection on proteins from different species: sequence convergence, and neutral rate violation (reviewed in ref. 1). Lysozymes from the stomachs of cows and langur monkeys, two mammalian species displaying fermentation in the foregut, are an example of amino-acid sequence convergence among homologous proteins. Here we combine tests of neutral rate violation with reconstruction of ancestral sequences to document an episode of positive selection on the lineage leading to the common ancestor of the foregut-fermenting colobine monkeys. This analysis also detected a previously unsuspected adaptive episode on the lineage leading to the common ancestor of the modern hominoid lysozymes. Both adaptive episodes were followed by episodes of negative selection. Thus this approach can detect adaptive and purifying episodes, and localize them to specific lineages during protein evolution.

Adaptation, Physiological↗