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      Mixed Fortunes: Ancient Expansion and Recent Decline in Population Size of a Subtropical Montane Primate, the Arunachal Macaque Macaca munzala

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          Abstract

          Quaternary glacial oscillations are known to have caused population size fluctuations in many temperate species. Species from subtropical and tropical regions are, however, considerably less studied, despite representing most of the biodiversity hotspots in the world including many highly threatened by anthropogenic activities such as hunting. These regions, consequently, pose a significant knowledge gap in terms of how their fauna have typically responded to past climatic changes. We studied an endangered primate, the Arunachal macaque Macaca munzala, from the subtropical southern edge of the Tibetan plateau, a part of the Eastern Himalaya biodiversity hotspot, also known to be highly threatened due to rampant hunting. We employed a 534 bp-long mitochondrial DNA sequence and 22 autosomal microsatellite loci to investigate the factors that have potentially shaped the demographic history of the species. Analysing the genetic data with traditional statistical methods and advance Bayesian inferential approaches, we demonstrate a limited effect of past glacial fluctuations on the demographic history of the species before the last glacial maximum, approximately 20,000 years ago. This was, however, immediately followed by a significant population expansion possibly due to warmer climatic conditions, approximately 15,000 years ago. These changes may thus represent an apparent balance between that displayed by the relatively climatically stable tropics and those of the more severe, temperate environments of the past. This study also draws attention to the possibility that a cold-tolerant species like the Arunachal macaque, which could withstand historical climate fluctuations and grow once the climate became conducive, may actually be extremely vulnerable to anthropogenic exploitation, as is perhaps indicated by its Holocene ca. 30-fold population decline, approximately 3,500 years ago. Our study thus provides a quantitative appraisal of these demographically important events, emphasising the ability to potentially infer the occurrence of two separate historical events from contemporary genetic data.

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          Most cited references31

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          Detection of reduction in population size using data from microsatellite loci.

          We demonstrate that the mean ratio of the number of alleles to the range in allele size, which we term M, calculated from a population sample of microsatellite loci, can be used to detect reductions in population size. Using simulations, we show that, for a general class of mutation models, the value of M decreases when a population is reduced in size. The magnitude of the decrease is positively correlated with the severity and duration of the reduction in size. We also find that the rate of recovery of M following a reduction in size is positively correlated with post-reduction population size, but that recovery occurs in both small and large populations. This indicates that M can distinguish between populations that have been recently reduced in size and those which have been small for a long time. We employ M to develop a statistical test for recent reductions in population size that can detect such changes for more than 100 generations with the post-reduction demographic scenarios we examine. We also compute M for a variety of populations and species using microsatellite data collected from the literature. We find that the value of M consistently predicts the reported demographic history for these populations. This method, and others like it, promises to be an important tool for the conservation and management of populations that are in need of intervention or recovery.
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            Rise and fall of the Beringian steppe bison.

            The widespread extinctions of large mammals at the end of the Pleistocene epoch have often been attributed to the depredations of humans; here we present genetic evidence that questions this assumption. We used ancient DNA and Bayesian techniques to reconstruct a detailed genetic history of bison throughout the late Pleistocene and Holocene epochs. Our analyses depict a large diverse population living throughout Beringia until around 37,000 years before the present, when the population's genetic diversity began to decline dramatically. The timing of this decline correlates with environmental changes associated with the onset of the last glacial cycle, whereas archaeological evidence does not support the presence of large populations of humans in Eastern Beringia until more than 15,000 years later.
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              Sampling for Microsatellite-Based Population Genetic Studies: 25 to 30 Individuals per Population Is Enough to Accurately Estimate Allele Frequencies

              One of the most common questions asked before starting a new population genetic study using microsatellite allele frequencies is “how many individuals do I need to sample from each population?” This question has previously been answered by addressing how many individuals are needed to detect all of the alleles present in a population (i.e. rarefaction based analyses). However, we argue that obtaining accurate allele frequencies and accurate estimates of diversity are much more important than detecting all of the alleles, given that very rare alleles (i.e. new mutations) are not very informative for assessing genetic diversity within a population or genetic structure among populations. Here we present a comparison of allele frequencies, expected heterozygosities and genetic distances between real and simulated populations by randomly subsampling 5–100 individuals from four empirical microsatellite genotype datasets (Formica lugubris, Sciurus vulgaris, Thalassarche melanophris, and Himantopus novaezelandia) to create 100 replicate datasets at each sample size. Despite differences in taxon (two birds, one mammal, one insect), population size, number of loci and polymorphism across loci, the degree of differences between simulated and empirical dataset allele frequencies, expected heterozygosities and pairwise FST values were almost identical among the four datasets at each sample size. Variability in allele frequency and expected heterozygosity among replicates decreased with increasing sample size, but these decreases were minimal above sample sizes of 25 to 30. Therefore, there appears to be little benefit in sampling more than 25 to 30 individuals per population for population genetic studies based on microsatellite allele frequencies.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                23 July 2014
                : 9
                : 7
                : e97061
                Affiliations
                [1 ]Nature Conservation Foundation, Gokulam Park, Mysore, India
                [2 ]National Centre for Biological Sciences, GKVK Campus, Bangalore, India
                [3 ]National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore, India
                Institut Pluridisciplinaire Hubert Curien, France
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DC AS UR. Performed the experiments: DC. Analyzed the data: DC. Contributed reagents/materials/analysis tools: UR. Wrote the paper: DC AS UR.

                Article
                PONE-D-13-16670
                10.1371/journal.pone.0097061
                4108313
                25054863
                fb53b734-3672-430e-bf56-71da181e10c4
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 8 April 2013
                : 14 April 2014
                Page count
                Pages: 11
                Funding
                The study was funded by a Department of Science and Technology, Government of India grant to AS, a Department of Biotechnology, Government of India grant to both UR and AS and an International Primatological Society research grant to DC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biogeography
                Ecology
                Ecological Metrics
                Population Size
                Effective Population Size
                Evolutionary Ecology
                Global Change Ecology
                Population Ecology
                Evolutionary Biology
                Evolutionary Genetics
                Population Genetics
                Population Biology
                Earth Sciences
                Atmospheric Science
                Climatology
                Climate Change
                Ecology and Environmental Sciences

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                Uncategorized

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