Genotyping of Capreolus pygargus fossil DNA from Denisova cave reveals phylogenetic relationships between ancient and modern populations

Background

The extant roe deer (Capreolus Gray, 1821) includes two species: the European roe deer (C. capreolus) and the Siberian roe deer (C. pygargus) that are distinguished by morphological and karyotypical differences. The Siberian roe deer occupies a vast area of Asia and is considerably less studied than the European roe deer. Modern systematics of the Siberian roe deer remain controversial with 4 morphological subspecies. Roe deer fossilized bones are quite abundant in Denisova cave (Altai Mountains, South Siberia), where dozens of both extant and extinct mammalian species from modern Holocene to Middle Pleistocene have been retrieved.

Methodology/Principal Findings

We analyzed a 629 bp fragment of the mitochondrial control region from ancient bones of 10 Holocene and four Pleistocene Siberian roe deer from Denisova cave as well as 37 modern specimen belonging to populations from Altai, Tian Shan (Kyrgyzstan), Yakutia, Novosibirsk region and the Russian Far East. Genealogical reconstructions indicated that most Holocene haplotypes were probably ancestral for modern roe deer populations of Western Siberia and Tian Shan. One of the Pleistocene haplotypes was possibly ancestral for modern Yakutian populations, and two extinct Pleistocene haplotypes were close to modern roe deer from Tian Shan and Yakutia. Most modern geographical populations (except for West Siberian Plains) are heterogeneous and there is some tentative evidence for structure. However, we did not find any distinct phylogenetic signal characterizing particular subspecies in either modern or ancient samples.

Conclusion/Significance

Analysis of mitochondrial DNA from both ancient and modern samples of Siberian roe deer shed new light on understanding the evolutionary history of roe deer. Our data indicate that during the last 50,000 years multiple replacements of populations of the Siberian roe deer took place in the Altai Mountains correlating with climatic changes. The Siberian roe deer represent a complex and heterogeneous species with high migration rates and without evident subspecies structure. Low genetic diversity of the West Siberian Plain population indicates a recent bottleneck or founder effect.     

Molecular genetic diversity of musk deer Moschus moschiferus L., 1758 (Ruminantia, Artiodactyla) from the northern subspecies group

Genetic diversity within the northern subspecies group of musk deer Moschus moschiferus L., 1758 was examined based on the mtDNA control region hypervariable fragment (300-bp) sequence polymorphism. Nucleotide diversity, constituting 2.6% for the whole sample (n = 34), varied in the range from 0.6 to 1.9% for individual subspecies. Maximum values of this index were observed for Siberian subspecies (M. m. moschiferus), which had the widest range. Genetic similarity between the haplotypes of the musk deer from the Far East (Russia) and Sakhalin Island, which grouped in one cluster in a phylogenetic tree, was demonstrated. The data obtained indicate that the distribution of musk deer along the territory of Russia occurred from Eastern Siberia to the Far East, and from there to the Sakhalin Island. A currently observed decrease of the musk deer population number along with the increased habitat fragmentation can result in a decrease of the total genetic diversity and in inbreeding depression in the local isolated groups.     

Phylogeography of the Siberian newt Salamandrella keyserlingii by mitochondrial DNA sequence analysis

Differentiation of geographical populations of the Siberian newt Salamandrella keyserlingii throughout the species range was analyzed using a fragment of the cytochrome b gene. The population of the Primorye region (Russian Far East) is separated to the greatest extent; the Japanese and South Kuril populations are the next most separate. These populations are possibly subspecies. Geographical differentiation of populations in the Siberian part of the species range is lower, lacks a clinal variation, and is irregular. The molecular variation of S. keyserlingii supports the hypothesis that several primary vicarious refugia of pre-Pleistocene differentiation of a common ancestor of Salamandrella occurred in the southeastern part of its current distribution range and that northern and western regions were gradually colonized via repeated steps of expansion and retreat in the Siberian part of the modern species range.     

Retrospective evaluation and modern state of the moose (<Emphasis Type="Italic">Alces alces</Emphasis> L.) population in West Siberia: Ecological and molecular-genetic aspects

Based on the analysis of materials collected for many years the dynamics of the moose’s habitat and population numbers in West Siberia is described. For the southeast of the West Siberian part of the habitat the cohabitation of mooses with the haplotypes of both European (A. a. alces L.) and East Siberian (A. a. pfizenmayeri Zukowski) subspecies is demonstrated on the basis of investigation of the structure of the mtDNA D-loop hypervariable domain. High nucleotide (p) and haplotypic (H) diversity substantially exceeding corresponding indices for the moose in the European part of Russia and the Urals has been revealed.     

Skull variation in the Siberian roe deer <Emphasis Type="Italic">Capreolus pygargus</Emphasis> from the Far East: a revision of the distribution of the subspecies

Extremely widespread in the Palaearctic, roe deer are heterogeneous in many ways including their morphology. At present, two roe deer species and four basic subspecies are acknowledged. The taxonomic system of the Siberian roe deer is poorly developed compared to that of the European roe deer. One of the principal points of roe deer systematics is the determination of the boundaries of the ranges of the roe deer subspecies requiring a thorough study of the species’ diversity. By using craniometry, one of the most adequate systematics techniques, we have analyzed geographical distribution of the Suberian roe deer in the Russian Far East and adjacent areas. All studied specimens were separated into three groups, the distributions of craniometric parameters of two of which did not overlap. One of the groups corresponds to Capreolus pygargus pygargus Pallas, 1771, while the other two do not correspond to any of the Siberian roe deer subspecies presently acknowledged. We have shown that the C. pygargus pygargus range extends to the east to the Northern Primorye, i.e., it is 2,000 to 3,000 km wider than previously believed. The subspecies status of Capreolus pygargus tianschanicus Satunin, 1906 was not confirmed. The Southern Primorye and left bank of the Amur River are thus a part of the range of Capreolus pygargus melanotis Miller, 1911, penetrating here from the Northeastern China.     

Structural Variation in the Nasal Bone Region of European Moose (Alces Alces L.)

The ontogeny of typical (normal) nasal bone region of the European moose (Alces alces L.) and the 3 variants of the pattern, was studied. The variants, named as “extra bone type”, “punctured type” and “open type” referring the morphology of the internasal suture, were originally observed in Finnish male and female moose skulls in 1971. All of the variants were later found in hunting trophy exhibitions presenting male moose trophies from Sweden, Norway, Baltic Republics of USSR and Poland. The frequencies of the variants showed regional differences. By using histological, radiological and OTC bone labelling methods, all of the nasal bone types were observed in this study in embryonal (N=36), newborn (N=21), juvenile (N=38) and adult (N=12) moose. Two twin embryos showed different nasal bone structure. The variation is considered to be of congenital origin.     

Genetic diversity of aboriginal and invasive populations of four‐eyed fir bark beetle Polygraphus proximus Blandford (Coleoptera,Curculionidae, Scolytinae)

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On the Gene Pool of Roe Deer (<Emphasis Type="Italic">Capreolus</Emphasis>) of Eastern Europe: Analysis of the Cyt <Emphasis Type="Italic">b</Emphasis> Gene Sequence Variability

Sequence analysis of the mtDNA cytochrome b gene (974 bp) was performed using 139 roe deer specimens from different regions of the European part of Russia and Ukraine. The data obtained showed that, at present, both European and Siberian roe deer inhabit this part of the range with predominance of the later: about 60% of individuals carry various Siberian haplotypes, most of which are similar to those in the populations of Capreolus pygargus from the Urals, Siberia, and the Far East. A great variety of mtDNA haplotypes of Siberian roe deer in Eastern Europe is undoubtedly caused by the heterogeneity of founder individuals (immigrants) that were imported from different parts of Asia. Some problems of coexistence of closely related species are discussed.     

Invasive alien plants of Russia: insights from regional inventories

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Cranometric Variability in Brown Bears of the Russian Far East

Morphometric analysis of 282 skulls of the brown bear Ursus arctos from the Far Eastern part of the range was carried out. The presence of two morphological clusters for both males and females is shown. Samples from two clusters were compared with their geographical location and subspecies. It was found that one cluster or another had no specific reference to the particular region or subspecies of a particular cluster, only the superiority of one over the other in a cluster of different subspecies and regions was changed. A comparison with the spread of brown bear genetic lines in the Far East of Russia is made. It was noted that the precise distribution of a particular cluster to a specific genetic line of haplotypes was not found.     

Genetic Diversity of Moose (Alces alces L.) in Eurasia

Polymorphism of nucleotide sequence of D-loop fragment of the mitochondrial DNA was studied in 20 moose from several local populations on the territory of Eurasia. Three main haplotype variants of D-loop were detected by molecular phylogenetic method, which formed three clusters named European, Asian, and American. Intraspecies variation in the length of HVSI of D-loop of the mitochondrial DNA of moose was revealed. In the Far Eastern and Yakutian moose, haplotypes with a 75-bp deletion were found, which were most similar with haplotypes (also with the deletion), earlier observed in North American moose [1]. The highest diversity of the haplotypes of mitochondrial DNA is characteristic of Yakutia and the Far East (where three haplotype variants were found), which demonstrates the probable role of the region as the center of the species origin or as the region of ancient population mixture. The geographic region might be considered as a probable source of ancient moose migrations from Asia to America, basing on the data of distribution of mitochondrial haplotypes of D-loop and alleles of MhcAlal-DRB1. Divergence of nucleotide sequences of haplotypes with the 75-bp deletion (forming the American cluster on the phylogenetic tree) was the lowest (0.4%), which evidences respectively recent origin of the group of haplotypes. In Europe, only haplotypes of mitochondrial DNA referred to European variant were observed. Basing on analysis of variation of nucleotide sequences of D-loop, exon 4 of -Casein and exon 2 of MhcAlal-DRB1, we demonstrated that Eurasian moose studied belong to the unique species, which has probably passed through a bottle neck. The time of the origin of modern diversity of D-loop haplotypes of the species was estimated as 0.075–0.15 Myr ago.     

Narrow phylogeographic origin of five introduced populations of the Siberian chipmunk Tamias (Eutamias) sibiricus (Laxmann, 1769) (Rodentia: Sciuridae) established in France

Large native geographical range and number of introduction events are often invoked to explain the successful establishment of alien mammal species. To infer the native geographic range of the Siberian chipmunks Tamias (Eutamias) sibiricus (Lax.) invasion in France, we identified the subspecies that individuals sampled in 5 out of the 11 established populations belonged. Based on craniometrical measures, variation in the mtDNA sequence of the cytochrome b, and alarm call sonogram shape, all French specimens were members of T. (E.) s. barberi which has the smallest geographical range (Korean peninsula) of the three recognized subspecies. An intense pet trade between European countries and Korea until the 1980’s best explains the success in establishment of this small ground-squirrel in France, where it was released mainly by private owners. Size of the native geographical range should be interpreted with caution in explaining the establishment of an invasive species, at least without a precise knowledge of its introduction pathways and taxonomic status.     

Molecular genetic diversity of musk deer Moschus moschiferus L., 1758 (Ruminantia, Artiodactyla) from the northern subspecies group

Genetic diversity within the northern subspecies group of musk deer Moschus moschiferus L, 1758 was examined based on the mtDNA control region hypervariable fragment (300-bp) sequence polymorphism. Nucleotide diversity, constituting 2.6% for the whole sample (n = 34), varied in the range from 0.6 to 1.9% for individual subspecies. Maximum values of this index were observed for Siberian subspecies (M. m. moschiferus), which had the widest range. Genetic similarity between the haplotypes of the musk deer from the Far East (Russia) and Sakhalin Island, which grouped in one cluster in a phylogenetic tree, was demonstrated. The data obtained indicate that the distribution of musk deer along the territory of Russia occurred from Eastern Siberia to the Far East, and from there to the Sakhalin Island. A currently observed decrease of the musk deer population number along with the increased habitat fragmentation can result in a decrease of the total genetic diversity and in inbreeding depression in the local isolated groups.     

Speciation in the stonechat (Saxicola torquata) inferred from nucleotide sequences of the cytochrome-b gene

The geographical differentiation and speciation in the stonechat (Saxicola torquata; Aves: Turdidae) was studied by sequencing a 300-bp fragment of the mitochondrial cytochrome-b gene. Stonechats from three different subspecies inhabiting three continents (S. t. rubicola, the European stonechat; S. t. maura, the Siberian stonechat; and S. t. axillaris, an African stonechat) and stonechats from seven European populations were examined. While variation within the populations of the European subspecies was less than 0.3%, the genetic distances between the subspecies were substantial (2.7-5.7%) in comparison with published data for subspecies of other birds. If speciation is indeed reflected in the cytochrome-b gene of stonechats, species status for the African stonechat, but also for the Siberian taxon, should be reconsidered, especially in the light of differences in distributions, morphology and habitat preference.     

Phylogeography of the Siberian newt (Salamandrella keyserlingii) by mitochondrial DNA sequence analysis

Differentiation of geographical populations of the Siberian newt Salamandrella keyserlingii throughout the species range was analyzed using a fragment of the cytochrome b gene. The population of the Primorye region (Russian Far East) is separated to the greatest extent; the Japanese and South Kuril populations are the next most separate. These populations are possibly subspecies. Geographical differentiation of populations in the Siberian part of the species range is lower, lacks a clinal variation, and is irregular. The molecular variation of S. keyserlingii supports the hypothesis that several primary vicarious refugia of pre-Pleistocene differentiation of a common ancestor of Salamandrella occurred in the southeastern part of its current distribution range and that northern and western regions were gradually colonized via repeated steps of expansion and retreat in the Siberian part of the modem species range.     

Phylogeography of the mallard Anas platyrhynchos from Eurasia inferred from sequencing of the mtDNA control region

Phylogenetic relationships, demographic history, and geographic distribution of the mtDNA haplotypes of the mallard Anas platyrhynchos were examined in three populations, Indian, Northern European, and Far Eastern. Two divergent halotype groups, A and B, were found in the Far Eastern population, while haplotypes identified in Northern European and Far Eastern populations were exclusively of the A group. The presence of B group haplotypes in the Far Eastern population can be explained either in terms of hybridization of the mallard with spot-billed duck Anas zonorhyncha at the south of the Russian Far East, or by the mtDNA paraphyly in mallards. In general, mallards from Eurasia were characterized by low genetic population differentiation along with slightly expressed phylogeographic structure. The most differentiated was the population from India (??_st = 0.076?0.077), while the difference between Northern European and Far Eastern populations was extremely low (??_st = 0.0029). Differentiation of Anas platyrhynchos Indian population was determined by the fact that a part of the population, inhabiting southern and eastern coasts of the Hindustan Peninsula, was resident.     

Intraspecific genetic differentiation of the Siberian Rubythroat (Luscinia calliope): Data of sequencing the mtDNA cytochrome b gene

For the first time, genetic diversity and intraspecific structure of Luscinia calliope was studied according to the data of the mtDNA cytochrome b gene sequencing. The strong differentiation of haplotypes of the Siberian Rubythroat into western and eastern groups, which include subspecies according to their geographical attachment, was revealed. A high-haplotypic (Hd = 0.986) and nucleotide (π= 0.00875) variety was shown for the species as a whole. We revealed considerable genetic distances (D = 0.016) between the western and eastern haplotypes that were four times higher than the intraspecific distances in terms of cytochrome b for passerines (D = 0.004). For three birds from Transbaikal, significant genetic divergence was detected, which could indirectly indicate the existence of the hybrid zone of several subspecies in this part of the area.     

Distribution of CCR5-delta 32 gene deletion across the Russian part of Eurasia

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Who Bites the Bullet First? The Susceptibility of Leopards Panthera pardus to Trophy Hunting

Reliable data is fundamentally important for managing large carnivore populations, and vital for informing hunting quota levels if those populations are subject to trophy hunting. Camera-trapping and spoor counts can provide reliable population estimates for many carnivores, but governments typically lack the resources to implement such surveys over the spatial scales required to inform robust quota setting. It may therefore be prudent to shift focus away from estimating population size and instead focus on monitoring population trend. In this paper we assess the susceptibility of African leopards Panthera pardus to trophy hunting. This has management ramifications, particularly if the use of harvest composition is to be explored as a metric of population trend. We explore the susceptibility of different leopard age and sex cohorts to trophy hunting; first by examining their intrinsic susceptibility to encountering trophy hunters using camera-traps as surrogates, and second by assessing their extrinsic susceptibility using photographic questionnaire surveys to determine their attractiveness to hunters. We show that adult male and female leopards share similar incident rates to encountering hunters but adult males are the most susceptible to hunting due to hunter preference for large trophies. In contrast, sub-adult leopards rarely encounter hunters and are the least attractive trophies. We suggest that our findings be used as a foundation for the exploration of a harvest composition scheme in the Kwazulu-Natal and Limpopo provinces where post mortem information is collected from hunted leopards and submitted to the local provincial authorities.     

Genetic variation and differentiation in striped field mouse <Emphasis Type="Italic">Apodemus agrarius</Emphasis> inferred from RAPD-PCR analysis

Genetic variation and differentiation of the trans-Palearctic species Apodemus agrarius (striped field mouse), whose range consists of two large isolates—European-Siberian and Far Eastern-Chinese, were examined using RAPD-PCR analysis. The material from the both parts of the range was examined (41 individual of A. agrarius from 18 localities of Russia, Ukraine, Moldova, and Kazakhstan); the Far Eastern-Chinese part was represented by samples from the Amur region, Khabarovsk krai, and Primorye (Russia). Differences in frequencies of polymorphic RAPD loci were found between the European-Siberian and the Far Eastern population groups of striped field mouse. No “fixed” differences between them in RAPD spectra were found, and none of the used statistical methods permitted to distinguish with absolute certainty animals from the two range parts. Thus, genetic isolation of the European-Siberian and the Far Eastern population groups of A. agrarius is not strict. These results support the hypothesis on recent dispersal of striped field mouse from East to West Palearctics (during the Holocene climatic optimum, 7000 to 4500 years ago) and subsequent disjunction of the species range (not earlier than 4000–4500 years ago). The Far Eastern population group is more polymorphic than the European-Siberian one, while genetic heterogeneity is more uniformly distributed within it. This is probably explained by both historical events that happened during the species dispersal in the past, and different environmental conditions for the species in different parts of its range. The Far Eastern population group inhabits the area close to the distribution center of A. agrarius. It is likely that this group preserved genetic variation of the formerly integral ancestral form, while some amount of genetic polymorphism could be lost during the species colonization of the Siberian and European areas. To date, the settlement density and population number in general are higher than within the European-Siberian isolate, which seems to account for closer interpopulation associations, intense genetic exchange, and “smoothing” of polymorphism within the Far Eastern population group of A. agrarius.