Millions of migratory birds occupy seasonally favourable breeding grounds in the Arctic 1 , but we know little about the formation, maintenance and future of Arctic bird migration routes and genetic determinants of migratory distance. Here, we established a continental-scale migration system, satellite tracking 56 peregrine falcons (Falco peregrinus) from six Eurasian Arctic breeding populations and resequencing 35 genomes from four of these. Different breeding populations used five migration routes across Eurasia, likely formed by longitude and latitude breeding ground shifts during the LGM-Holocene transition. Contemporary inter-route environmental divergence appears to maintain distinct migration routes. We found that the novel gene ADCY8 was associated with population-level migratory distance differences. We elucidated its regulatory mechanism and found the most likely selective agent for this divergence was long-term memory. Global warming is predicted to influence migration strategies and diminish breeding ranges of Eurasian Arctic peregrines. Harnessing ecological interactions and evolutionary processes to study climate-driven changes in migration can facilitate the conservation of migratory birds.
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 Correspondence: Xiangjiang Zhan, Fax: +86 (0)1064807099; E-mail: zhanxj@ioz.ac.cn 1 These two authors contributed equally to the paper. highland adaptation involve relatively few genes, but are nonetheless more complex than previously thought and involve fine-tuned transcriptional responses and genomic adaptation.
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