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Molecules support morphology: species status of South Indian populations of the widely distributed Hanuman langur
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The taxonomy of the Hanuman langur (Sem-nopithecus spp.), a widely distributed Asian colobine monkey, has been in a flux for a long time due to much disagreement between various classification schemes. However, results from a recent field-based morphological study were consistent with Hill's (Ceylon J Sci 21:277–305, 1939) species level classification scheme. Here we tested the validity of S. hypoleucos and S. priam, the two South Indian species recognized by Hill. To this end, one mitochondrial and four nuclear markers were sequenced from over 72 non-invasive samples of Hanuman langurs and S. johnii collected from across India. The molecular data were subjected to various tree building methods. The nuclear data was also used in a Bayesian structure analysis and to determine the genealogical sorting index of each hypothesized species. Results from nuclear data suggest that the South Indian population of Hanuman langur consists of two units that correspond to the species recognized by Hill. However in the mitochondrial tree S. johnii and S. priam were polyphyletic probably due to retention of ancestral polymorphism and/or low levels of hybridization. Implications of these results on conservation of Hanuman langurs are also discussed.
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... The Tapti-Godavari rivers in central India form the borderline with NT distributed to the north and ST distributed to the south of these rivers (Roonwal, 1979(Roonwal, , 1984. Recent studies support the splitting of ST Hanuman langur into two species, namely Semnopithecus priam Blyth, 1844 and Semnopithecus hypoleucos Blyth, 1841, based on an integrative approach wherein multiple lines of evidence from molecular, morphological, and ecological data were used (Ashalakshmi et al., 2014;Nag et al., 2011Nag et al., , 2014. Similarly, genetic and morphological data suggest that the plains population of NT Hanuman langur is a separate species, Semnopithecus entellus Dufresne, 1797 (Karanth et al., 2010). ...
... With the advent of molecular techniques many recent studies have used genetic data to resolve taxonomic ambiguities in primates of the Indian subcontinent (Arekar et al., 2019;Ashalakshmi et al., 2014;Chakraborty et al., 2007;Karanth et al., 2008Karanth et al., , 2010Osterholz et al., 2008;Wangchuk et al., 2008). However, the use of molecular data does not guarantee a robust description and identification . ...
... iucnr edlist.org). We included our field data as well as published sequences from previous studies (Ashalakshmi et al., 2014;Karanth et al., 2010;Khanal et al., 2018). ...
Taxonomy is replete with groups where the species identity and classification remain unresolved. One such group is the widely distributed Hanuman langur (Colobinae: Semnopithecus). For most part of the last century, the Hanuman langur was considered to be a single species with multiple subspecies. Nevertheless, recent studies using an integrative taxonomy approach suggested that this taxon is a complex, with at least three species. However, these studies did not include the Himalayan population of the Hanuman langur whose taxonomic status remains unresolved. The Himalayan population of Hanuman langurs has been classified as a distinct species with multiple subspecies or been subsumed into other species. These classification schemes are wholly based on morphological characters which are sometimes insufficient to delimit different species. Here, we have integrated data from multiple sources viz. morphology, DNA, and ecology to resolve the taxonomy of the Himalayan langur and to understand its distribution limit. Our results with three lines of evidence corresponding to three different species concepts show that Himalayan langur is a species distinct from Semnopithecus entellus of the plains. Additionally, these results did not show any support for splitting of the Himalayan langur into multiple subspecies. Our study supports the classification proposed by Hill (Ceylon Journal of Science, XXI, 1939) and we recommend Semnopithecus schistaceus Hodgson, 1840 as species name for the Himalayan langur and subsume all the known subspecies into it.
... show the occurrence of two species, i.e. black-footed gray langur Semnopithecus hypoleucos and gray-tufted Langur Semnopithecus priam in the Western Ghats [12][13][14] . We added rhesus macaque and two species of langurs instead of one species of Hanuman langur to the list of primates. ...
... M. silenus are confined to a narrow strip of rainforests south of Aghanashini River in the central Western Ghats to the southern tip of the hill system 27,28 . The northern limit of the distribution range of Nilgiri langurs S. johnii marks Brahmagiri Hills in the central Western Ghats, whereas S. hypoleucos replaces the same niche at the north of these hills, and S. priam occupies the rainshadow areas, especially the eastern slopes of the Western Ghats 12,14,28 . ...
An updated list confirms the presence of 134 species of wild mammals in the Western Ghats, India. The superimposed distribution range of all, and threatened species of mammals depicts the potential mammalian key diversity areas for the Western Ghats, which can be prioritized for long-term conservation. These mammalian key diversity areas are confined to the central and the southern Western Ghats. The most crucial key diversity areas for both threatened and all mammalian species occur in Pushpagiri-Talakaveri, the Nilgiri Biosphere, the Anamalai Hills, the Periyar landscape and the Agas-tyamalai Hills.
... These studies have enabled researchers to identify a range of directly observable and cryptic hybridization phenomena that played a role in the evolutionary diversification of this subfamily. For example, morphological (coloration), bioacoustic, and molecular evidence suggest both observable hybridization and cryptic introgression of genes between ecologically distinct langurs that co-inhabit the mosaic of evergreen and deciduous forest in the south of Indian subcontinent (Semnopithecus johnii, S. priam, and possibly S. hypoleucos) (Hohman, 1988;Ashalakshmi et al., 2015;Nag, 2020). Hybridization between Semnopithecus priam thersites and S. vetulus in Sri Lanka is supported by behavioral evidence and observation of coat color pattern (Lu et al., 2020). ...
Interspecific hybridization in primates is common but hybridization between distantly related sympatric primate species is rarely observed in the wild. We present evidence for a possible hybridization event between Nasalis larvatus and Trachypithecus cristatus in the Lower Kinabatangan Wildlife Sanctuary, Sabah, through assessment of photographs. We used a set of categorical characters and metric measurements to compare the putative hybrid with the likely parent species. Nonmetric comparison showed that this "mystery monkey" is intermediate in several characters. Measurements of limb proportions on photographs showed that the brachial, humerofemoral, and intermembral indexes are above 100 for N. larvatus and below 100 for T. cristatus on all photographs, whereas the crural index is higher than 100 in both species and the distributions of this index in the two species overlap. Brachial and intermembral indices of the putative hybrid were similar to those of N. larvatus. Crural and humerofemoral indices were closer to the values for T. cristatus than those of N. larvatus. Multiple observers confirmed the occurrence of mixed-species groups in the area, and interspecific mating has been photographed. The putative hybrid is now an adult female and was last photographed in September 2020 with an infant and swollen breast, suggesting lactation. We propose further noninvasive fecal sampling for genetic analyses to confirm the origins of this "mystery monkey." This case of hybridization may be related to anthropogenic changes to the landscape, whereby expansion of oil palm plantations confines N. larvatus and T. obscurus to narrow riverine forest patches along the Kinabatangan. This observation therefore also may have conservation implications, indicating limited mate access and dispersal opportunities for these threatened primates.
Supplementary information:
The online version contains supplementary material available at 10.1007/s10764-022-00293-z.
... These two genera together have the highest species diversity among all the colobine genera (Roos et al. 2014). There has been much controversy in the taxonomy of these two genera (Oates et al. 1994;Groves 2001;Brandon-Jones et al. 2004); however, with the advent of molecular tools many of these issues have been resolved Ashalakshmi et al. 2014;Arekar et al. 2021). Yet, the taxonomic placement of two species, currently in the genus Trachypithecus, continues to be in debate; these include the endangered golden langur (Trachypithecus geei) and capped langur (Trachypithecus pileatus). ...
The phylogenetic position of the capped and golden langur (CG) lineage has been ambiguous owing to the discordance between phylogenies from multiple molecular markers. Previous molecular studies have hypothesised that this discordance likely arises from either a hybridization event that took place between the Indian genus Semnopithecus and the Southeast Asian genus Trachypithecus or from incomplete lineage sorting (ILS). Distinguishing between hybridization and ILS is challenging and these processes can lead to serious difficulties in inferring phylogenies. In this study, we used genetic markers (nine nuclear and eight mitochondrial) in conjunction with coalescent based species tree approach and a test for hybridization using posterior predictive checking to better understand the evolutionary origin of the CG lineage. Both the concatenated nuclear as well as the mitochondrial dataset recovered congruent relationships where CG lineage was sister to Trachypithecus. However, nuclear species tree estimated using different multispecies coalescent methods suggested an opposite result, i.e. CG lineage was sister to Semnopithecus. Hybridization analysis strongly indicates gene flow between Semnopithecus and Trachypithecus that likely gave rise to the hybrid CG lineage. Further, the CG lineage is morphologically intermediate between Semnopithecus and Trachypithecus with respect to skull and body measurements. In light of the above evidences, we argue that the CG lineage needs to be elevated to a new genus of its own. Taxonomic and conservation implications of these results are also discussed.
... Gray langurs (Semnopithecus entellus), commonly called Hanuman langurs have colonized various parts of the Indian subcontinent, ranging from the desert to forest fringes, and have lived with a diversified resource structure and human interference (Oppenheimer, 1977;Ashalakshmi et al., 2014;Chetan et al., 2014). In comparison to the other species of langur, social organization of the gray langur is highly flexible (Newton, 1988;Caton, 1999;Sterck, 1999;Rajpurohit et al., 2006) and is often modified by the male-male competition followed by infanticides (Hrdy, 1974;Broom et al., 2004;Sharma et al., 2010). ...
... Gray langurs (Semnopithecus entellus), commonly called Hanuman langurs have colonized various parts of the Indian subcontinent, ranging from the desert to forest fringes, and have lived with a diversified resource structure and human interference (Oppenheimer, 1977;Ashalakshmi et al., 2014;Chetan et al., 2014). In comparison to the other species of langur, social organization of the gray langur is highly flexible (Newton, 1988;Caton, 1999;Sterck, 1999;Rajpurohit et al., 2006) and is often modified by the male-male competition followed by infanticides (Hrdy, 1974;Broom et al., 2004;Sharma et al., 2010). ...
Urbanization affects concurrent human-animal interactions as a result of altered resource availability and land use pattern, which leads to considerable ecological consequences. While some animals have lost their habitat due to urban encroachment, few of them managed to survive within the urban ecosystem by altering their natural behavioral patterns. The feeding repertoire of folivorous colobines, such as gray langur, largely consists of plant parts. However, these free-ranging langurs tend to be attuned to the processed high-calorie food sources to attain maximum benefits within the concrete jungle having insignificant greenery. Therefore, besides understanding their population dynamics, the effective management of these urbanized, free-ranging, non-human primate populations also depends on their altered feeding habits. Here, we have used a field-based experimental setup that allows gray langurs to choose between processed and unprocessed food options, being independent of any inter-specific conflicts over resources due to food scarcity. The multinomial logit model reveals the choice-based decision-making of these free-ranging gray langurs in an urban settlement of West Bengal, India, where they have not only learned to recognize the human-provisioned processed food items as an alternative food source but also shown a keen interest in it. However, such a mismatch between the generalized feeding behavior of folivorous colobines and their specialized gut physiology reminds us of Liem's paradox and demands considerable scientific attention. While urbanization imposes tremendous survival challenges to these animals, it also opens up for various alternative options for surviving in close proximity to humans which is reflected in this study, and could guide us for the establishment of a sustainable urban ecosystem in the future.
... Gray langurs (Semnopithecus entellus), commonly called Hanuman langurs have colonized various parts of the Indian subcontinent, ranging from the desert to forest fringes, and have lived with a diversified resource structure and human interference (Oppenheimer, 1977;Ashalakshmi et al., 2014;Chetan et al., 2014). In comparison to the other species of langur, social organization of the gray langur is highly flexible (Newton, 1988;Caton, 1999;Sterck, 1999;Rajpurohit et al., 2006) and is often modified by the male-male competition followed by infanticides (Hrdy, 1974;Broom et al., 2004;Sharma et al., 2010). ...
Population size and geographical range are the key quantitative criteria used by the IUCN to assess the conservation status of a species. However, such information is often incomplete and inconsistent, even for seemingly abundant species. To assess the population and conservation status of Indian primates, we conducted a systematic review of recent research using the searching, appraisal, synthesis and analysis (SALSA) approach. We reviewed a total of 41 studies on Indian primates conducted during the last 2 decades (2000–2021) for information on various parameters that influence their conservation. We found that 20 out of a total of 26 primate species were evaluated for their population status, and the majority of these studies (71%) showed an overall declining population trend. Remarkably, all but one of the studies conducted exclusively within protected areas revealed declining population trends, whereas trends were more variable for primate populations in non-protected areas. Our data indicate that only 27% (n = 7) of Indian primate species have been surveyed or re-surveyed to assess their population status within the last 5 years. Although threats vary in time and space from species to species, 78% of the studies recorded natural system modifications including habitat loss and fragmentation among the main threats to the survival of Indian primates. Most studies on the population status of Indian primates have either been spatially limited or used outdated methods. We recommend that future studies adopt robust techniques to estimate populations and work across larger geographical scales to develop effective management strategies for the conservation of primates in India.
The Colobines are a group of Afroeurasian monkeys that exhibit extraordinary behavioural and ecological diversity. With long tails and diverse colourations, they are medium-sized primates, mostly arboreal, that are found in many different habitats, from rain forests and mountain forests to mangroves and savannah. Over the last two decades, our understanding of this group of primates has increased dramatically. This volume presents a comprehensive overview of the current research on colobine populations, including the range of biological, ecological, behavioural and societal traits they exhibit. It highlights areas where our knowledge is still lacking, and outlines the current conservation status of colobine populations, exploring the threats to their survival. Bringing together international experts, this volume will aid future conservation efforts and encourage further empirical studies. It will be of interest to researchers and graduate students in primatology, biological anthropology and conservation science. Additional online resources can be found at www.cambridge.org/colobines.
The term “integrative taxonomy”, or the use of multiple lines of evidence in the delimitation and naming of new species, was independently introduced in two papers in 2005. This paper aims to provide a brief review of integrative taxonomy and the growth of molecular tools in systematics, with special reference to its prevalence and scope for biodiversity research in India. We review the literature to understand the state of progress in systematics from India since 2005 using both vertebrate and invertebrate examples. We end by summarising best practises and a workflow for integrative taxonomy, as well as emphasizing the need for a national strategy for taxonomy and systematic research with an outline on how to achieve this.
We describe extensions to the method of Pritchard et al. for inferring population structure from multilocus genotype data. Most importantly, we develop methods that allow for linkage between loci. The new model accounts for the correlations between linked loci that arise in admixed populations (“admixture linkage disequilibium”). This modification has several advantages, allowing (1) detection of admixture events farther back into the past, (2) inference of the population of origin of chromosomal regions, and (3) more accurate estimates of statistical uncertainty when linked loci are used. It is also of potential use for admixture mapping. In addition, we describe a new prior model for the allele frequencies within each population, which allows identification of subtle population subdivisions that were not detectable using the existing method. We present results applying the new methods to study admixture in African-Americans, recombination in Helicobacter pylori, and drift in populations of Drosophila melanogaster. The methods are implemented in a program, structure, version 2.0, which is available at http://pritch.bsd.uchicago.edu.
An accurately resolved gene tree may not be congruent with the species tree because of lineage sorting of ancestral polymorphisms. DNA sequences from the mitochondrially encoded genes (mtDNA) are attractive sources of characters for estimating the phylogenies of recently evolved taxa because mtDNA evolves rapidly, but its utility is limited because the mitochondrial genes are inherited as a single linkage group (haplotype) and provide only one independent estimate of the species tree. In contrast, a set of nuclear genes can be selected from distinct chromosomes, such that each gene tree provides an independent estimate of the species tree. Another aspect of the gene-tree versus species-tree problem, however, favors the use of mtDNA for inferring species trees. For a three-species segment of a phylogeny, the branching order of a gene tree will correspond to that of the species tree if coalescence of the alleles or haplotypes occurred in the internode between the first and second bifurcation. From neutral theory, it is apparent that the probability of coalescence increases as effective population size decreases. Because the mitochondrial genome is maternally inherited and effectively haploid, its effective population size is one-fourth that of a nuclear-autosomal gene. Thus, the mitochondrial-haplotype tree has a substantially higher probability of accurately tracking a short internode than does a nuclear-autosomal-gene tree. When an internode is sufficiently long that the probability that the mitochondrial-haplotype tree will be congruent with the species tree is 0.95, the probability that a nuclear-autosomalgene tree will be congruent is only 0.62. If each of k independently sampled nuclear-gene trees has a probability of congruence with the species tree of 0.62, then a sample of 16 such trees would be required to be as confident of the inference based on the mitochondrial-haplotype tree. A survey of mtDNA-haplotype diversity in 34 species of birds indicates that coalescence is generally very recent, which suggests that coalescence times are typically much shorter than internodal branch lengths of the species tree, and that sorting of mtDNA lineages is not likely to confound the species tree. Hybridization resulting in transfer of mtDNA haplotypes among branches could also result in a haplotype tree that is incongruent with the species tree; if undetected, this could confound the species tree. However, hybridization is usually easy to detect and should be incorporated in the historical narrative of the group, because reticulation, as well as cladistic events, contributed to the evolution of the group.
We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.
Occurrence of langurs with an aberrant coat colour has been reported for different places in the Western Ghats, south India. Analyses of loud calls of a so-called "brown langur' male revealed a similar physical structure to equivalent vocal pattenrs of both Nilgiri langur and common langur. -from Author
— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.