title: Population transcriptomes reveal synergistic responses of DNA polymorphism and RNA expression to extreme environments on the Qinghai-Tibetan Plateau in a predatory bird.
abstract: Low oxygen and temperature pose key physiological challenges for endotherms living on the Qinghai-Tibetan Plateau (QTP). Molecular adaptations to high-altitude living have been detected in the genomes of Tibetans, their domesticated animals and a few wild species, but the contribution of transcriptional variation to altitudinal adaptation remains to be determined. Here we studied a top QTP predator, the saker falcon, and analysed how the transcriptome has become modified to cope with the stresses of hypoxia and hypothermia. Using a hierarchical design to study saker populations inhabiting grassland, steppe/desert and highland across Eurasia, we found that the QTP population is already distinct despite having colonized the Plateau <2000 years ago. Selection signals are limited at the cDNA level, but of only seventeen genes identified, three function in hypoxia and four in immune response. Our results show a significant role for RNA transcription: 50% of upregulated transcription factors were related to hypoxia responses, differentiated modules were significantly enriched for oxygen transport, and importantly, divergent EPAS1 functional variants with a refined co-expression network were identified. Conservative gene expression and relaxed immune gene variation may further reflect adaptation to hypothermia. Our results exemplify synergistic responses between DNA polymorphism and RNA expression diversity in coping with common stresses, underpinning the successful rapid colonization of a top predator onto the QTP. Importantly, molecular mechanisms underpinning highland adaptation involve relatively few genes, but are nonetheless more complex than previously thought and involve fine-tuned transcriptional responses and genomic adaptation.
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.|Institute of Zoology Joint Laboratory for Biocomplexity Research, Cardiff University, Beichen West Road, Beijing, 100101, China.|University of Chinese Academy of Sciences, Yuquan Road, Beijing, 100049, China.
authors.forename: Shengkai
authors.initials: S
authors.lastname: Pan
authors.affiliation: Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810008, China.
authors.forename: Tongzuo
authors.initials: T
authors.lastname: Zhang
authors.affiliation: Beijing Honortech Co. Ltd., Beijing, 102200, China.
authors.forename: Zhengqin
authors.initials: Z
authors.lastname: Rong
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.|University of Chinese Academy of Sciences, Yuquan Road, Beijing, 100049, China.|BGI-Shenzhen, Shenzhen, 518083, China.
authors.forename: Li
authors.initials: L
authors.lastname: Hu
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.|University of Chinese Academy of Sciences, Yuquan Road, Beijing, 100049, China.
authors.forename: Zhongru
authors.initials: Z
authors.lastname: Gu
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.
authors.forename: Qi
authors.initials: Q
authors.lastname: Wu
authors.affiliation: Key Laboratory of Biomedical Information Engineering of Ministry of Education, School of Life Science and Technology, Xi'an Jiaotong University, Xi'an, 710049, China.
authors.forename: Shanshan
authors.initials: S
authors.lastname: Dong
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.|State Key Laboratory of Earth Surface Processes and Resource Ecology & MOE Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Qiong
authors.initials: Q
authors.lastname: Liu
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.
authors.forename: Zhenzhen
authors.initials: Z
authors.lastname: Lin
authors.affiliation: Raptor Protection of Slovakia, Kuklovská 5, SK-841 04, Bratislava 4, Slovakia.
authors.forename: Lucia
authors.initials: L
authors.lastname: Deutschova
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.
authors.forename: Xinhai
authors.initials: X
authors.lastname: Li
authors.affiliation: Institute of Zoology Joint Laboratory for Biocomplexity Research, Cardiff University, Beichen West Road, Beijing, 100101, China.|International Wildlife Consultants Ltd., PO Box 19, Carmarthen, SA33 5YL, UK.|Environment Agency-Abu Dhabi, PO Box 45553, Al Mamoura Building (A), Muroor Road, Abu Dhabi, United Arab Emirates.
authors.forename: Andrew
authors.initials: A
authors.lastname: Dixon
authors.affiliation: Institute of Zoology Joint Laboratory for Biocomplexity Research, Cardiff University, Beichen West Road, Beijing, 100101, China.|Organisms and Environment Division, Cardiff School of Bioscience, Cardiff University, Cardiff, CF10 3AX, UK.
authors.forename: Michael W
authors.initials: MW
authors.lastname: Bruford
authors.affiliation: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Beijing, 100101, China.|Institute of Zoology Joint Laboratory for Biocomplexity Research, Cardiff University, Beichen West Road, Beijing, 100101, China.
authors.forename: Xiangjiang
authors.identifier: http://orcid.org/0000-0002-4517-1626
authors.initials: X
authors.lastname: Zhan
mesh_terms: D000531:Altitude; D000818:Animals; D000071251:Extreme Environments; D046093:Falconiformes / Q000235:genetics*; D005828:Genetics, Population; D011110:Polymorphism, Genetic; D012313:RNA / Q000235:genetics; D018609:Tibet; D059467:Transcriptome
chemical_list: D012313:RNA
keywords: Qinghai-Tibetan Plateau; RNA sequencing; adaptation; colonization; population transcriptome; saker falcon