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30 September 2022, Volume 42 Issue 5

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Viewpoints of the wildlife conservation biology research on the Qinghai-Tibet Plateau

Fuwen WEI

2022, 42(5):  475-476.  DOI: 10.16829/j.slxb.150734

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The Qinghai?Tibet Plateau, as an important ecological barrier in China, is a natural laboratory for wildlife conservation biology research due to the uniqueness and richness in animal resources. Although the wildlife conservation researches have made great achievements in this area, we could further strengthen the following three aspects benefited from the development of science and technology. First, the long-term monitoring of wildlife populations and habitats on the plateau should be maintained; Second, multi and crossing disciplines and macro and micro points of view should be combined to conduct integrative biology researches; Third, the training of youth scientists for the wildlife conservation on the plateau should be further strengthened.

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Research advance and perspective on mammalogy in Northwest Institute of Plateau Biology, Chinese Academy of Sciences

Jianghui BIAN, Dehua WANG

2022, 42(5):  477-481.  DOI: 10.16829/j.slxb.150718

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The year 2022 marks the 60th anniversary (1962?2022) of the establishment of Northwest Institute of Plateau Biology (NWIPB), Chinese Academy of Sciences. The mammalogy research of NWIPB has also gone through the course of 60 years, which has experienced the continuous development and expansion process from nothing to nothing. Over the past 60 years, the research in mammalogy at NWIPB has always been based on the Qinghai?Tibet Plateau, based on basic research and basic application research. To meet the needs of the state, serve for the regional economy and ecological protection, a large number of corresponding work has been carried out on mammalogy, a large number of scientific and technological talents have been cultivated, several academic publictions have been published by NWIPB，which has made a significant contribution to the development of mammalogy and mammalogy ecology.

REVIEWS

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Physiological Ecology of Small Mammals in Qinghai‒Tibetan Plateau: from individual to ecosystem

Dehua WANG, Zuwang WANG

2022, 42(5):  482-489.  DOI: 10.16829/j.slxb.150722

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We reviewed the development and advances in physiological ecology of small mammals on the Qinghai?Tibetan Plateau, including the characteristics of energy metabolism and physiological adaptation the environment, adaptive thermogenesis and thermoregulation, energy balance and body weight regulation, physiological limits, populations energy flow, and recent advances in some new areas, such as using double-labeled water method to measure energy expenditure in free?living animals, geographic physiology, physiological function of gut microbiota, plant secondary metabolites and their physiological functions, and population physiology. Several works such as ecological energetics, adaptive thermogenesis, and physiological adaptation have been leading the development of animal physiological ecology in China. We also proposed some possible directions and areas for development and enhancement in physiological ecology for alpine small mammals in the future in order to establish and enrich the discipline of Physiological Ecology of Small Mammals on the Qinghai?Tibetan Plateau.

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Research advances in conservation and management of endangered mammals on the Qinghai-Tibet Plateau

Tongzuo ZHANG, Feng JIANG, Bo XU, Bin LI, Chengbo LIANG, Haifeng GU

2022, 42(5):  490-507.  DOI: 10.16829/j.slxb.150696

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The Qinghai-Tibet Plateau (QTP) is a global biodiversity hotspot and a priority area for conservation.It hosts a variety of key protected and endemic wildlife species, contributing to a high level of species richness and a large proportion of endangered species. We reviewed the research advances in the conservation and management of 7 fauna groups on the Qinghai-Tibet Plateau (ungulates, felids, ursids, canids, mustelids, chiropterans, and other small mammals) from the perspectives of the endangered status, threatening causes, strategies and effects of conservation and management. The proportion of endemic species of ungulates was much higher than that of the other 6 groups. 81% ? 100% of ungulate, felid, ursid, and canid species were listed as the national key protected wildlife. 45% to 100% of ungulate, felid, and ursid species were listed as threatened by the Red List of China’s Vertebrates or Red List of IUCN, which is far higher than the global average. Habitat fragmentation, global warming, overgrazing, poaching and illegal trade, and environmental pollution were the major threats to the survival of endangered mammals on the QTP. The implementation of relevant laws and policies, the construction of nature reserves, as well as the carrying out of a large number of investigations, monitoring, and researches have provided legal guarantees and scientific basis for the conservation and management of endangered mammals on the QTP. In view of the limitations of current conservation and management, we suggest building a comprehensive and systematic big data platform, so as to conduct rapid assessment of conservation effectiveness on the QTP and research on spatial optimization of protected areas. We also suggest combining internationally advanced interdisciplinary theoretical methods and practical innovation to provide guidance and suggestions for the protection and management of endangered mammals, so as to provide important scientific and technical support for the biodiversity conservation and ecological civilization construction of China.

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Research advances in conservation genetics and genomics of snow leopard (Panthera uncia)

Yubo HAO, Hong JIN, Lin YANG, Kexin LI, Yibo HU

2022, 42(5):  508-518.  DOI: 10.16829/j.slxb.150687

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The snow leopard (Panthera uncia) (Carnivora, Felidae, Panthera) is a flagship species distributed in the Qinghai?Tibet Plateau and surrounding regions. With the development of molecular biology and high-throughput sequencing technology, snow leopard conservation genetics and conservation genomics have developed rapidly. Noninvasive genetic sampling has provided genetic samples and facilitated the conservation genetics research of snow leopards. In this review, we summarize the application of noninvasive genetic sampling in species identification, individual identification and sex determination of snow leopards, the phylogenetic status, phylogeographic pattern, population genetic structure, and subspecies controversies in snow leopards. Furthermore, the evolutionary history, adaptive evolution, and genome characteristics of snow leopards are reviewed. Finally, we discuss the future development trends of snow leopard conservation genetics and genomics, aiming to better promote snow leopard conservation biology research and science-based conservation decisions.

ORIGINAL PAPERS

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Effects of captivity on the assembly process of microbiota communities of plateau pikas

Liangzhi ZHANG, Xianjiang TANG, Shien Ren, Yaqi ZHAO, Yanming ZHANG

2022, 42(5):  519-530.  DOI: 10.16829/j.slxb.150721

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Revealing the community assembly process is helpful to better understand the mechanism of biodiversity generation and maintenance, which has been an emerging topic in microbial community ecology in recent years. Studies have shown that captivity can cause drastic changes in the composition and diversity of intestinal microbiotas, however, whether captivity can alter the assembly processes of gut bacterial communities in plateau pikas is still unknown. Here, we employed 16S rRNA gene-based large-scale structural profiling to explore the effect of captivity and breeding status on the gut microbial composition, diversity, functions, and assembly processes in plateau pikas (Ochotona curzoniae). The results showed that the community richness and community coverage index of captivity animals were significantly lower than those of wild groups. For the wild groups, the indexes were significantly higher in non-breeding groups than those of breeding groups. The relative abundance of Bacteroidetes was significantly higher in the captivity group than that of the wild groups, while the relative abundance of Firmicutes and Planctomycetes were significantly higher in wild groups than those of the captivity group. For the wild groups, the richness of Epsilonbacteraeota and Tenericutes were higher in the breeding period group than those of the non-breeding group. The results of functional prediction revealed that the abundance of genes involved in cardiovascular disease and cell communication were significantly different between captivity and wild breeding groups. The abundance of genes involved in the pathway of amino acid metabolism, carbohydrate metabolism, and lipid metabolism enriched in non-breeding groups compared with breeding groups. The results of neutral model revealed that captivity reduced the importance of stochastic processes in governing the bacterial community assembly, while breeding status increased the importance of stochastic processes in structuring the community assembly. Our results provided new insights on the effects of captivity on the microbial composition, diversity, function, and assembly processes and the interactions between microbiotas and physiological state of plateau pika, which provided a new theoretical basis to promote the possibility of successful reproduction in laboratory.

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Grassland degradation affects serum total IgG level, intestinal parasitic infection and liver and kidney indices of plateau pika

Xueqin WU, Huiqing CHEN, Lu ZHANG, Guozhen SHANG, Yan WU, Jianghui BIAN

2022, 42(5):  531-539.  DOI: 10.16829/j.slxb.150715

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As a key species in the alpine grassland ecosystem of the Qinghai?Tibet Plateau, the plateau pika (Ochotona curzoniae) population increased rapidly with grassland degradation. Understanding the changes in innate immune function and organ index of liver and kidney indices of plateau pika is of great significance for further revealing the physiological mechanism of plateau pika population outbreak caused by grassland degradation on the Qinghai?Tibet Plateau. In this study, we investigated the number of burrow entrances, measured serum total IgG levels, intestinal parasitic infection, and liver and kidney indices of adult plateau pikas inhabiting lightly, moderately, and heavily degraded grassland (LD, MD and HD) at Qinghai Haibei National Field Research Station of Alpine Grassland Ecosystem. Our results showed that with grassland degradation, the number of burrow entrances and serum total IgG levels increased significantly, while the prevalence and intensity of infection of cestodes and nematodes as well as liver and kidney indices decreased markedly. The prevalence of infection of cestodes and liver index in males were significantly lower than those in females, and the prevalence and intensity of infection of cestodes and nematodes in females in HD were significantly lower than those in LD. These results indicate that grassland degradation induced by overgrazing enhances the innate immune of plateau pika and alleviate the damage of toxins to liver and kidney, which may promote population outbreaks.

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Association between personality and SERT gene polymorphisms in plateau pikas (Ochotona curzoniae) at different altitudes

Hongjuan ZHU, Jing LI, Suqin WANG, Qi TANG, Xianyong LAN, Jiapeng QU

2022, 42(5):  540-552.  DOI: 10.16829/j.slxb.150702

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Given the stable and heritable individual differences in animal behaviors, personality is associated with the polymorphisms of related genes and reflects the adaptation patterns of animals to variable environments. Exploring the variations in personality-related genes will contribute to the improved understanding of the evolutionary and adaptation mechanisms of animals’ response to environments. In this study, we used plateau pikas (Ochotona curzoniae) inhabiting five altitudinal regions of the Qinghai–Tibetan Plateau as study objects to determine their personality variations, explore the associations between single nucleotide polymorphisms (SNP) of serotonin transporter (SERT) and personality, and obtain the expression level of the SERT gene. Results showed that the exploration and boldness of pikas at high altitudes were significantly higher than those at low altitudes, whereas the expression level of SERT at high altitudes was significantly lower than that at low altitudes, suggesting that the personality of pikas in different altitudes might be correlated with the mRNA expression of the SERT gene. Furthermore, SERT gene polymorphisms and their distribution differences among different altitudes were detected. Six SNP mutations were detected in the SERT gene (5 and 1 SNP mutations were located in exons 3 and 5, respectively). Significant correlations between c.A1063C synonymous mutation in exon 5 and altitudes were observed, suggesting that the distribution frequencies of the CC genotype of c.A1063C at high altitudes were significantly higher than those at low altitudes. No significant correlation between c.A1063C genotypes and exploration or boldness was observed, whereas significant correlations between c.A1063C genotypes and docility were detected. Our results suggested that with increasing altitude, the exploration and boldness of plateau pikas increased for food resource and survival opportunities to adapt to environments at different altitudes and that the difference in docility might be related to the synonymous mutation of exon 5 of the SERT gene c.A1063C. This study attempted to elaborate on the differences in personality of plateau pikas adapted to different altitudes from the perspective of gene expression and mutation, providing the potential molecular mechanism of plateau pika’s behavioral strategies at different altitudes.

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Habitat suitability evaluation of snow leopard ( Panthera uncia ) in the Qilian Mountain National Park (Qinghai area), China

Zhanlei RONG, Yayue GAO, Shengyun CHEN, Tongzuo ZHANG

2022, 42(5):  553-562.  DOI: 10.16829/j.slxb.150545

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Snow leopard (Panthera uncia) is a flagship species for global biodiversity conservation. Accurate assessment of snow leopard habitat quality can provide scientific reference for population conservation. In this study, we assess the habitat suitability of snow leopards in the Qilian Mountain National Park (Qinghai area) using landscape connectivity analyses and MaxEnt model. The main environmental factors such as topography, climate, landcover type, and human disturbance were selected. The results showed that highly suitable habitat was mainly distributed in the west and middle of the study area, which comprisesand 71.8% ? 77.5% of the Qinghai area. The overlap area of the suitable habitat predicted by the two methods was 8 979.1 km², representing 56.7% of the Qinghai area. The suitable habitat accounts for 39.8% ? 43.3% of the general control area and 56.7% ? 60.2% of the core reserve. The maximum area of suitable habitat is distributed in the Shule River Basin and the minimal area is distributed in the Shiyang River Basin. The highest proportion of suitable habitat is located in the Heihe River Basin, which was about 77.1% ? 91.8%. The suitable habitat showed an increasing trend from east to west and we detected a large area of snow leopard habitat in the general control area. Human activities will be a potential threat to the snow leopard habitat in the general control area. This study provides a scientific reference for optimizing in situ protection measures for snow leopards.

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Risk of transmission and infection of gastrointestinal parasites in the Tibetan antelope (Pantholops hodgsonii) aggregation

Yifan CAO, Guozhen SHANG, Wenjing LI, Yuangang YANG, Tong WU, Yahui ZHU, Jianghui BIAN, Ruiqiang ZHANG, Tongzuo ZHANG, Xinquan ZHAO

2022, 42(5):  563-571.  DOI: 10.16829/j.slxb.150556

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Herbivores aggregation is beneficial to reduce the predation risk but it can also increase the transmission and infection risk of parasites. Zhuonai Lake, located in Hoh Xil, Qinghai Province, an important calving ground of Tibetan antelope (Pantholops hodgsonii). The aggregating time of Tibetan antelope in Zhuonai Lake area is mainly concentrated from early June to July (less than 30 days).Climate factors such as temperature and humidity in this region might have an important impact on the development of parasite eggs/oocysts in the host’s feces. In this study, a microclimate observer was constructed in the calving ground of Zhuonai Lake to collect local meteorological data on June 9th, 2018. In this area, fresh feces of Tibetan antelope were collected and placed outdoors for 0, 10, 15, 20, 25, 30, 35 days, and nearly one year (300 days). We used the flotation technique to detect the development status of eggs/oocysts in different periods within 35 days and the species of surviving larvae in the feces placed outdoors for nearly one year. Our aim was to preliminarily test the development, hatching, and overwintering survival of the dominant parasite eggs/oocysts in the feces of aggregated Tibetan antelope in the Zhuonai Lake area and evaluate whether the calving ground increases the risk of gastrointestinal parasite transmission and infection in Tibetan antelope. The results showed that: (1) between June 9 and July 16, the 35 days average temperature was 5℃ and the average relative humidity was 81%. (2) During the aggregating period of Tibetan antelope in Zhuonai Lake area (less than 30 days), the dominant parasite eggs/oocysts in the feces did not develop to the infective stage (Third larvae stage). For example, dominant nematode eggs, including Trichostrongylus sp., Marshallagia sp., and Nematodirus sp., only developed to the first larvae stage within 30 days. Additionally, the sporulation rates of dominant coccidian species Eimeria pantholopensis and E. wudaoliangensis were 0, 18.9 %, 54.0 % and 0, 13.5 %, 30.4 % on the 25th days, 30th days, and 35th days, respectively. (3) Few parasite eggs survived over the winter until the next year. Only a few larvae of the Marshallagia sp. and Nematodirus sp. were found in feces which were placed for nearly one year to survive over the winter in the calving ground of Zhuonai Lake. This study suggests that the risk of gastrointestinal parasite transmission and infection was low during the aggregating period of Tibetan antelope in Zhuonai Lake area. Short-term utilization of calving ground and rapid back-migration were important behavioral strategies for Tibetan antelope to avoid increasing the risk of gastrointestinal parasitic infection. Furthermore, the climate environment such as low temperature was beneficial to the natural purification of parasites.

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Expression analysis of gap junction protein 40 in lung of plateau pika exposed to hypoxia

Xuze ZHANG, Lin FU, Xiaoyan ZOU, Yurong DU

2022, 42(5):  572-578.  DOI: 10.16829/j.slxb.150686

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Blunted hypoxic pulmonary vasoconstriction response is a major adaptation to hypoxia in plateau pika (Ochotona curzoniae). However, the genes involved in this physiological compensation remained unclear. In the present study, plateau pikas and Sprague Dawley (SD) rats were challenged with a hypoxia condition simulating an altitude of 5 000 m for 28 days. Morphological structure analysis by immunohistochemistry was carried out for the pulmonary in both species and the expression levels of Connexin40 (Cx40), a member of the Connexon family expressed in pulmonary vascular endothelia in mammals, were determined by both qPCR and Western blot. The results showed that upon hypoxia challenge the alveoli of plateau pika appeared to be vacuolated sacs. Cx40 expression was detected in both bronchi and pulmonary blood vessels in both species. In plateau pikas, mRNA level of Cx40 increased after hypoxia challenge, while its protein level decreased. In contrast, protein levels of Cx40 had no significant change with prolonged hypoxia exposure in pulmonary blood vessels of SD rats. No significant change in the Cx40 protein in the lung bronchi was observed in both species. Our results indicate that with hypoxia exposure, pulmonary vasoconstriction response in plateau pikas could be suppressed by down-regulation of Cx40, contributing to their adaptation to a hypoxic environment on the plateau. Our results can provide a reference for the expression analysis of gap junction proteins in the lungs of indigenous animals living on the Qinghai-Tibet Plateau.

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Effects of hypobaric hypoxia on spermatogenesis and the expression of small RNA in mice

Shuang LI, Gongxue JIA, Haiping TAO, Yujun WANG, Binye LI, Qien YANG

2022, 42(5):  579-589.  DOI: 10.16829/j.slxb.150649

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As the most crucial environmental factors, low atmospheric pressure and low oxygen content have adverse effects on the reproductive system of non-adapted animals living in the Qinghai?Tibet Plateau. Compelling evidence has shown that hypoxia exposure caused increased germ cell apoptosis and lower sperm quality, leading to defects in fertilization and preimplantation embryo development. Currently, how hypoxia affects testicular gene expression and sperm function is not well-understood. small RNA regulates gene expression at the post-transcriptional and translational level and participates in spermatogenesis by inducing gene silencing or transcription. In this study, a hypoxia mouse model was established by simulating the environment at an altitude of 5 000 m in a hypobaric oxygen chamber for 4 weeks. The results showed that the germ cells within seminiferous tubules of hypoxic mice were arranged disorderly. Although the total number of sperm did not change significantly, the proportion of abnormal sperm had a 17.5 fold increase in Hypo-4W animals (P < 0.001). small RNA sequencing revealed that the number of small RNAs with a length of 21 nt in hypoxic mouse sperm was reduced by 4.4% (P < 0.05), and the first base had a strong preference for Uracil (U). There were no significant differences in piRNA and tsRNA in sperm of control and hypoxia exposed animals, however, 21 miRNAs were up-regulated and 58 were down-regulated. Furthermore, we analyzed the target genes of these miRNAs and differentially expressed genes in the hypoxia-treated testicular tissues of mice. The results showed that 429 target genes of up-regulated miRNAs and 813 target genes of down-regulated miRNAs were differentially expressed. Finally, enrichment analysis revealed that the target genes of up-regulated miRNAs were enriched in FoxO signaling pathway, thyroid hormone signaling pathway, steroid biosynthesis and HIF-1 signaling pathway, while the targets of down-regulated miRNAs were enriched in fatty acid metabolism. In summary, the miRNA expression dynamics of hypoxic mouse sperm obtained in the present study provides an important reference value for further dissecting changes in sperm epigenome in humans and other animals under hypoxic environment.

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Effects of hypoxia stress on liver function and gene expression in mice

Haiping TAO, Shuang LI, Gongxue JIA, Luyao ZHANG, Yougui FANG, Yongwei CHEN, Qien YANG

2022, 42(5):  590-600.  DOI: 10.16829/j.slxb.150697

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As one of the most characteristic environmental factors on the Qinghai-Tibet Plateau, hypoxia has a profound impact on the adaptive evolution of plateau animals. Continued exposure to a hypoxic environment causes metabolic dysfunction of the body. In non-acclimated animals, long-term hypoxia exposure affects liver function, but there is still a lack of knowledge regarding its effect on offspring liver. In this study, adult mice were transferred to a high altitude hypoxic environment (altitude 3 220 m) for breeding. Mice reared under normoxic conditions were used as a control and the growth and live function of hypoxic-treated mice (hypoxic generation 0) and their offspring (hypoxic generation 1 ? generation 5) were evaluated.The results showed that long-term hypoxia exposure led to morphological and functional changes in the liver. Hepatocytes of hypoxia-exposed animals were swollen, caused by red blood cells infiltrating between hepatic cords. Specifically, the fatty degeneration appeared in the liver lobules of hypoxic generation 1 mice. Blood biochemical analyses showed that compared with the normoxia generation 0, the levels of alanine aminotransferase and aspartate aminotransferase in hypoxia generation 0 and hypoxia generation 1 increased significantly (P < 0.05).Albumin, globulin, total bilirubin and total cholesterol levels decreased in hypoxia generation 0 and increase in hypoxia generation 1 (P < 0.05). After fasting injection of glucose and insulin, the glucose tolerance and insulin sensitivity of mice in the hypoxic group were greatly reduced (P < 0.05). RNA-seq analysis of liver tissue from normoxic generation 0, hypoxic generation 0, and hypoxic generation 1 identified 459 differential expression genes (DEGs) in livers of hypoxia-exposed animals. These genes were significantly enriched in the MAPK signaling pathway, apoptosis, lipid metabolism, and endoplasmic reticulum pathway. This study demonstrated that hypoxic exposure has important effects on the liver in mice and the outcomes of these findings provide information to further elucidate the physiological and pathological changes induced by hypoxia at high altitudes.

SCIENTIFIC NOTES

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The utilization of wildlife passages by migratory Tibetan antelope in Sanjiangyuan National Park: a case study of Wubei Bridge of Qinghai‒Tibet Railway

gaowa Saiqing, Hongqi LI, Dong WANG, Zihan WANG, Xinming LIAN

2022, 42(5):  601-608.  DOI: 10.16829/j.slxb.150670

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The Qinghai?Tibet Railway (QTR) crosses the migration routes of the Tibetan antelope (Pantholops hodgsonii) in the Sanjiangyuan National Park (SNP) and the female antelopes have to cross the QTR by wildlife passages to continue their migrations. In this study, a remote monitoring camera was set up near the Wubei Bridge to record the utilization of the bridge by migratory antelopes. Based on the monitoring data of the returning migration period from July to September 2019 and the calving migration period from April to June 2020, the results showed that: Tibetan antelopes crossed the Wubei Bridge mainly in the daytime and mostly in the morning. The peaks during the calving migration and the returning migration were in 09: 00?12: 59 and 11: 00?11: 59 respectively. Compared with the returning migration period, female antelopes gathered into smaller groups during the calving migration period, which was related to the sequence of roads to be crossed and the lower predation risk of calves in larger groups. We found individuals in larger groups spent less time crossing the Wubei Bridge. Larger groups could accelerate crossing speed and then reduce the average crossing time of individuals. However, there was no significant difference in the average crossing time of individuals between the two migratory periods, indicating that the presence of calves had little effect on the speed and time of antelope groups. In conclusion, there was a significant difference in the group size of Tibetan antelope between the returning and calving migration periods and the group size affected the average crossing time of individuals. We also detected a temporal pattern in the use of wildlife passage by Tibetan antelope.

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Genetic diversity of male specific region of Y chromosome in Tibetan antelope

Ruotong CHENG, Yibo CHEN, Xiangqiong MENG, Jiarui CHEN, Qing WEI

2022, 42(5):  609-614.  DOI: 10.16829/j.slxb.150688

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Genetic diversity is an important indicator of population health, especially for assessing population recovery of endangered species. To characterize the genetic diversity of Tibetan antelope(Pantholops hodgsonii) populations, we used muscle and placental tissues from accidentally killed Tibetan antelopes in Qinghai and Xinjiang and screened 11 Tibetan antelope Y-SNP-specific loci from 30 published polymorphic Y-SNP loci in bovids, of which AMELY3 (g.723 C > T) and SRYOY1 (g.167 G > A) 2 pairs of primers were polymorphic. Based on the AMELY3 locus, the haplotype diversity of Tibetan antelope Y chromosome was 0.048 ± 0.045 and the nucleotide polymorphism was 0.00006 ± 0.00005. According to the SRYOY1 locus, Tibetan antelope was divided into two haplotypes, of which H1 (g.167 G) was the dominant haplotype. Maximum likelihood tree suggests that Tibetan antelope might have two paternal origins. The haplotype diversity of Tibetan antelope Y chromosome was 0.439 ± 0.050 and the nucleotide polymorphism was 0.0008 ± 0.0004. The genetic differentiation index showed that the F_ST value between the male population of Tibetan antelope in Qinghai and Xinjiang was 0.6846 ± 0.0389, suggesting a strong population genetic differentiation. Therefore, integrated conservation across regions and research on sex chromosomes need more attention in the future conservation of Tibetan antelope.