Climate-driven flyway changes and memory-based long-distance migration.

Millions of migratory birds occupy seasonally favourable breeding grounds in the Arctic1, but we know little about the formation, maintenance and future of the migration routes of Arctic birds and the genetic determinants of migratory distance. Here we established a continental-scale migration system that used satellite tracking to follow 56 peregrine falcons (Falco peregrinus) from 6 populations that breed in the Eurasian Arctic, and resequenced 35 genomes from 4 of these populations. The breeding populations used five migration routes across Eurasia, which were probably formed by longitudinal and latitudinal shifts in their breeding grounds during the transition from the Last Glacial Maximum to the Holocene epoch. Contemporary environmental divergence between the routes appears to maintain their distinctiveness. We found that the gene ADCY8 is associated with population-level differences in migratory distance. We investigated the regulatory mechanism of this gene, and found that long-term memory was the most likely selective agent for divergence in ADCY8 among the peregrine populations. Global warming is predicted to influence migration strategies and diminish the breeding ranges of peregrine populations of the Eurasian Arctic. Harnessing ecological interactions and evolutionary processes to study climate-driven changes in migration can facilitate the conservation of migratory birds.

Global patterns of human-wildlife spatial associations and implications for differentiating conservation strategies.

Understanding the global patterns of human and wildlife spatial associations is essential for pragmatic conservation implementation, yet analytical foundations and indicator-based assessments that would further this understanding are lacking. We integrated the global distributions of 30,664 terrestrial vertebrates and human pressures to map human-nature index (HNI) categories that indicate the extent and intensity of human-wildlife interactions. Along the 2 dimensions of biodiversity and human activity, the HNI allowed placement of terrestrial areas worldwide in one of 4 HNI categories: anthropic (human-dominated areas), wildlife-dominated (little human influence and rich in wildlife), co-occurring (substantial presence of humans and wildlife), and harsh-environment (limited presence of humans and wildlife) areas. The HNI varied considerably among taxonomic groups, and the leading driver of HNI was global climate patterns. Co-occurring regions were the most prevalent (35.9%), and wildlife-dominated and anthropic regions encompassed 26.45% and 6.50% of land area, respectively. Our results highlight the necessity for customizing conservation strategies to regions based on human-wildlife spatial associations and the distribution of existing protected area networks. Human activity and biodiversity should be integrated for complementary strategies to support conservation toward ambitious and pragmatic 30×30 goals.

Patrones globales de las asociaciones espaciales entre humanos y fauna y las implicaciones para la diferenciación de las estrategias de conservación Resumen Es esencial entender los patrones globales de asociaciones entre humanos y fauna para la implementación pragmática de la conservación. Aun así, son muy pocos los fundamentos analíticos y las evaluaciones basadas en indicadores que incrementarían este conocimiento. Integramos la distribución global de 30,664 vertebrados terrestres y presiones humanas para mapear las categorías del índice de naturaleza humana (INH) que indican la extensión e intensidad de las interacciones humano­fauna. El INH permitió la colocación de áreas terrestres en todo el mundo en las dos dimensiones de la biodiversidad y las actividades humanas dentro de una de las cuatro categorías del INH: áreas antrópicas (dominadas por humanos), dominadas por fauna (poca influencia humana y rica en fauna), co­ocurrentes (presencia sustancial de humanos y fauna) y de ambiente severo (presencia limitada de humanos y fauna). El INH varió considerablemente entre los taxones, y el factor principal fueron los patrones climáticos mundiales. Las regiones co­ocurrentes fueron las más frecuentes (35.9%) las regiones antrópicas y dominadas por fauna englobaron el 26.45% y 6.50% del área terrestre respectivamente. Nuestros resultados enfatizan la necesidad de personalizar las estrategias de conservación acorde a la región con base en las asociaciones espaciales entre humanos y fauna y la distribución de las redes existentes de áreas protegidas. La actividad humana y la biodiversidad deberían estar integradas para las estrategias complementarias para respaldar a la conservación hacia los objetivos ambiciosos y pragmáticos de 30 para el 30.

Evolutionary Conservation Genomics Reveals Recent Speciation and Local Adaptation in Threatened Takins.

Incorrect species delimitation will lead to inappropriate conservation decisions, especially for threatened species. The takin (Budorcas taxicolor) is a large artiodactyl endemic to the Himalayan-Hengduan-Qinling Mountains and is well known for its threatened status and peculiar appearance. However, the speciation, intraspecies taxonomy, evolutionary history, and adaptive evolution of this species still remain unclear, which greatly hampers its scientific conservation. Here, we de novo assembled a high-quality chromosome-level genome of takin and resequenced the genomes of 75 wild takins. Phylogenomics revealed that takin was positioned at the root of Caprinae. Population genomics based on the autosome, X chromosome, and Y chromosome SNPs and mitochondrial genomes consistently revealed the existence of two phylogenetic species and recent speciation in takins: the Himalayan takin (B. taxicolor) and the Chinese takin (B. tibetana), with the support of morphological evidence. Two genetically divergent subspecies were identified in both takin species, rejecting three previously proposed taxonomical viewpoints. Furthermore, their distribution boundaries were determined, suggesting that large rivers play important roles in shaping the genetic partition. Compared with the other subspecies, the Qinling subspecies presented the lowest genomic diversity, higher linkage disequilibrium, inbreeding, and genetic load, thus is in urgent need of genetic management and protection. Moreover, coat color gene (PMEL) variation may be responsible for the adaptive coat color difference between the two species following Gloger's rule. Our findings provide novel insights into the recent speciation, local adaptation, scientific conservation of takins, and biogeography of the Himalaya-Hengduan biodiversity hotspot.

RNA-combine: a toolkit for comprehensive analyses on transcriptome data from different sequencing platforms.

BACKGROUND: Understanding the transcriptome has become an essential step towards the full interpretation of the biological function of a cell, a tissue or even an organ. Many tools are available for either processing, analysing transcriptome data, or visualizing analysis results. However, most existing tools are limited to data from a single sequencing platform and only several of them could handle more than one analysis module, which are far from enough to meet the requirements of users, especially those without advanced programming skills. Hence, we still lack an open-source toolkit that enables both bioinformatician and non-bioinformatician users to process and analyze the large transcriptome data from different sequencing platforms and visualize the results. RESULTS: We present a Linux-based toolkit, RNA-combine, to automatically perform the quality assessment, downstream analysis of the transcriptome data generated from different sequencing platforms, including bulk RNA-seq (Illumina platform), single cell RNA-seq (10x Genomics) and Iso-Seq (PacBio) and visualization of the results. Besides, this toolkit is implemented with at least 10 analysis modules more than other toolkits examined in this study. Source codes of RNA-combine are available on GitHub: https://github.com/dongxuemin666/RNA-combine . CONCLUSION: Our results suggest that RNA-combine is a reliable tool for transcriptome data processing and result interpretation for both bioinformaticians and non-bioinformaticians.

Rapid Spread of Severe Fever with Thrombocytopenia Syndrome Virus by Parthenogenetic Asian Longhorned Ticks.

Severe fever with thrombocytopenia syndrome virus (SFTSV) is spreading rapidly in Asia. This virus is transmitted by the Asian longhorned tick (Haemaphysalis longicornis), which has parthenogenetically and sexually reproducing populations. Parthenogenetic populations were found in ≥15 provinces in China and strongly correlated with the distribution of severe fever with thrombocytopenia syndrome cases. However, distribution of these cases was poorly correlated with the distribution of populations of bisexual ticks. Phylogeographic analysis suggested that the parthenogenetic population spread much faster than bisexual population because colonization is independent of sexual reproduction. A higher proportion of parthenogenetic ticks was collected from migratory birds captured at an SFTSV-endemic area, implicating the contribution to the long-range movement of these ticks in China. The SFTSV susceptibility of parthenogenetic females was similar to that of bisexual females under laboratory conditions. These results suggest that parthenogenetic Asian longhorned ticks, probably transported by migratory birds, play a major role in the rapid spread of SFTSV.

Transcription-Associated Mutation Promotes RNA Complexity in Highly Expressed Genes-A Major New Source of Selectable Variation.

Alternatively spliced transcript isoforms are thought to play a critical role for functional diversity. However, the mechanism generating the enormous diversity of spliced transcript isoforms remains unknown, and its biological significance remains unclear. We analyzed transcriptomes in saker falcons, chickens, and mice to show that alternative splicing occurs more frequently, yielding more isoforms, in highly expressed genes. We focused on hemoglobin in the falcon, the most abundantly expressed genes in blood, finding that alternative splicing produces 10-fold more isoforms than expected from the number of splice junctions in the genome. These isoforms were produced mainly by alternative use of de novo splice sites generated by transcription-associated mutation (TAM), not by the RNA editing mechanism normally invoked. We found that high expression of globin genes increases mutation frequencies during transcription, especially on nontranscribed DNA strands. After DNA replication, transcribed strands inherit these somatic mutations, creating de novo splice sites, and generating multiple distinct isoforms in the cell clone. Bisulfate sequencing revealed that DNA methylation may counteract this process by suppressing TAM, suggesting DNA methylation can spatially regulate RNA complexity. RNA profiling showed that falcons living on the high Qinghai-Tibetan Plateau possess greater global gene expression levels and higher diversity of mean to high abundance isoforms (reads per kilobases per million mapped reads ≥18) than their low-altitude counterparts, and we speculate that this may enhance their oxygen transport capacity under low-oxygen environments. Thus, TAM-induced RNA diversity may be physiologically significant, providing an alternative strategy in lifestyle evolution.

Mitochondrial complex I bridges a connection between regulation of carbon flexibility and gastrointestinal commensalism in the human fungal pathogen Candida albicans.

Efficient assimilation of alternative carbon sources in glucose-limited host niches is critical for colonization of Candida albicans, a commensal yeast that frequently causes opportunistic infection in human. C. albicans evolved mechanistically to regulate alternative carbon assimilation for the promotion of fungal growth and commensalism in mammalian hosts. However, this highly adaptive mechanism that C. albicans employs to cope with alternative carbon assimilation has yet to be clearly understood. Here we identified a novel role of C. albicans mitochondrial complex I (CI) in regulating assimilation of alternative carbon sources such as mannitol. Our data demonstrate that CI dysfunction by deleting the subunit Nuo2 decreases the level of NAD+, downregulates the NAD+-dependent mannitol dehydrogenase activity, and consequently inhibits hyphal growth and biofilm formation in conditions when the carbon source is mannitol, but not fermentative sugars like glucose. Mannitol-dependent morphogenesis is controlled by a ROS-induced signaling pathway involving Hog1 activation and Brg1 repression. In vivo studies show that nuo2Δ/Δ mutant cells are severely compromised in gastrointestinal colonization and the defect can be rescued by a glucose-rich diet. Thus, our findings unravel a mechanism by which C. albicans regulates carbon flexibility and commensalism. Alternative carbon assimilation might represent a fitness advantage for commensal fungi in successful colonization of host niches.

Population transcriptomes reveal synergistic responses of DNA polymorphism and RNA expression to extreme environments on the Qinghai-Tibetan Plateau in a predatory bird.

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.

Genetics, morphology and ecology reveal a cryptic pika lineage in the Sikkim Himalaya.

Asian pika species are morphologically ∼similar and have overlapping ranges. This leads to uncertainty and species misidentification in the field. Phylogenetic analyses of such misidentified samples leads to taxonomic ambiguity. The ecology of many pika species remains understudied, particularly in the Himalaya, where sympatric species could be separated by elevation and/or substrate. We sampled, measured, and acquired genetic data from pikas in the Sikkim Himalaya. Our analyses revealed a cryptic lineage, Ochotona sikimaria, previously reported as a subspecies of O. thibetana. The results support the elevation of this lineage to the species level, as it is genetically divergent from O. thibetana, as well as sister species, O. cansus (endemic to central China) and O. curzoniae (endemic to the Tibetan plateau). The Sikkim lineage diverged from its sister species' about 1.7-0.8myrago, coincident with uplift events in the Himalaya. Our results add to the recent spate of cryptic diversity identified from the eastern Himalaya and highlight the need for further study within the Ochotonidae.

Genetics and Evolution of Bird Migration.

Bird migration has long been a subject of fascination for humankind and is a behavior that is both intricate and multifaceted. In recent years, advances in technology, particularly in the fields of genomics and animal tracking, have enabled significant progress in our understanding of this phenomenon. In this review, we provide an overview of the latest advancements in the genetics of bird migration, with a particular focus on genomics, and examine various factors that contribute to the evolution of this behavior, including climate change. Integration of research from the fields of genomics, ecology, and evolution can enhance our comprehension of the complex mechanisms involved in bird migration and inform conservation efforts in a rapidly changing world.

Genetic consequences of historical anthropogenic and ecological events on giant pandas.

The giant panda (Ailuropoda melanoleuca) was taken to the brink of extinction in the 1980s through a combination of deforestation, large-scale loss of bamboo in the core of its range, poaching, and zoo collection, causing over 1000 deaths from the 1950s. It was thought that the drastic population decline was likely to impose a severe impact on population viability. Here, based on temporal genotyping of individuals, we show that this rapid decline did not significantly reduce the overall effective population size and genetic variation of this species, or of the two focal populations (Minshan and Qionglai) that declined the most. These results are contrary to previously assumptions, probably because the population decline has not produced the expected negative impact due to the short time scale involved (at most 10 generations), or because previous surveys underestimated the population size at the time of decline. However, if present-day habitat fragmentation and limited migration of giant pandas remains, we predict a loss of genetic diversity across the giant pandas' range in the near future. Thus, our findings highlight the substantial resilience of this species when facing demographic and environmental stochasticity, but key conservation strategies, such as enhancing habitat connectivity and habitat restoration should be immediately implemented to retain the extant genetic variation and maintain long-term evolutionary potential of this endangered species.

Whole-genome survey reveals extensive variation in genetic diversity and inbreeding levels among peregrine falcon subspecies.

In efforts to prevent extinction, resource managers are often tasked with increasing genetic diversity in a population of concern to prevent inbreeding depression or improve adaptive potential in a changing environment. The assumption that all small populations require measures to increase their genetic diversity may be unwarranted, and limited resources for conservation may be better utilized elsewhere. We test this assumption in a case study focused on the peregrine falcon (Falco peregrinus), a cosmopolitan circumpolar species with 19 named subspecies. We used whole-genome resequencing to generate over two million single nucleotide polymorphisms (SNPs) from multiple individuals of all peregrine falcon subspecies. Our analyses revealed extensive variation among subspecies, with many island-restricted and nonmigratory populations possessing lower overall genomic diversity, elevated inbreeding coefficients (F ROH)-among the highest reported, and extensive runs of homozygosity (ROH) compared to mainland and migratory populations. Similarly, the majority of subspecies that are either nonmigratory or restricted to islands show a much longer history of low effective population size (N e). While mutational load analyses indicated an increased proportion of homozygous-derived deleterious variants (i.e., drift load) among nonmigrant and island populations compared to those that are migrant or reside on the mainland, no significant differences in the proportion of heterozygous deleterious variants (i.e., inbreeding load) was observed. Our results provide evidence that high levels of inbreeding may not be an existential threat for some populations or taxa. Additional factors such as the timing and severity of population declines are important to consider in management decisions about extinction potential.

Black and white and read all over: the past, present and future of giant panda genetics.

Few species attract much more attention from the public and scientists than the giant panda (Ailuropoda melanoleuca), a popular, enigmatic but highly endangered species. The application of molecular genetics to its biology and conservation has facilitated surprising insights into the biology of giant pandas as well as the effectiveness of conservation efforts during the past decades. Here, we review the history of genetic advances in this species, from phylogeny, demographical history, genetic variation, population structure, noninvasive population census and adaptive evolution to reveal to what extent the current status of the giant panda is a reflection of its evolutionary legacy, as opposed to the influence of anthropogenic factors that have negatively impacted this species. In addition, we summarize the conservation implications of these genetic findings applied for the management of this high-profile species. Finally, on the basis of these advances and predictable future changes in genetic technology, we discuss future research directions that seem promising for giant panda biology and conservation.

SARS-CoV-2 RNAs are processed into 22-nt vsRNAs in Vero cells.

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has caused the global pandemic, resulting in great fatalities around the world. Although the antiviral roles of RNA interference (RNAi) have been well studied in plants, nematodes and insects, the antiviral roles of RNAi in mammalians are still debating as RNAi effect is suspected to be suppressed by interferon (IFN) signaling pathways in most cell types. To determine the role of RNAi in mammalian resistance to SARS-CoV-2, we studied the profiling of host small RNAs and SARS-CoV-2 virus-derived small RNAs (vsRNAs) in the early infection stages of Vero cells, an IFN-deficient cell line. We found that host microRNAs (miRNAs) were dysregulated upon SARS-CoV-2 infection, resulting in downregulation of microRNAs playing antiviral functions and upregulation of microRNAs facilitating viral proliferations. Moreover, vsRNA peaked at 22 nt at negative strand but not the positive strand of SARS-CoV-2 and formed successive Dicer-spliced pattern at both strands. Similar characteristics of vsRNAs were observed in IFN-deficient cell lines infected with Sindbis and Zika viruses. Together, these findings indicate that host cell may deploy RNAi pathway to combat SARS-CoV-2 infection in IFN-deficient cells, informing the alternative antiviral strategies to be developed for patients or tissues with IFN deficiency.

Arctic introgression and chromatin regulation facilitated rapid Qinghai-Tibet Plateau colonization by an avian predator.

The Qinghai-Tibet Plateau (QTP), possesses a climate as cold as that of the Arctic, and also presents uniquely low oxygen concentrations and intense ultraviolet (UV) radiation. QTP animals have adapted to these extreme conditions, but whether they obtained genetic variations from the Arctic during cold adaptation, and how genomic mutations in non-coding regions regulate gene expression under hypoxia and intense UV environment, remain largely unknown. Here, we assemble a high-quality saker falcon genome and resequence populations across Eurasia. We identify female-biased hybridization with Arctic gyrfalcons in the last glacial maximum, that endowed eastern sakers with alleles conveying larger body size and changes in fat metabolism, predisposing their QTP cold adaptation. We discover that QTP hypoxia and UV adaptations mainly involve independent changes in non-coding genomic variants. Our study highlights key roles of gene flow from Arctic relatives during QTP hypothermia adaptation, and cis-regulatory elements during hypoxic response and UV protection.

Molecular evidence for Pleistocene refugia at the eastern edge of the Tibetan Plateau.

The role of the Quaternary ice ages in forming the contemporary genetic structure of populations has been well studied in a number of global regions. However, due to the different nature of glaciations and complex topography, their role in shaping eastern Eurasian genetic diversity, particular in areas surrounding the Tibetan Plateau have remained largely unstudied. We aimed to address this question by examining the genetic structure of an alpine forest-associated taxon, the blood pheasant (Ithaginis cruentus) to infer its phylogeographic history. We detected three phylogenetic lineages and four current population groups. By comparing molecular and palaeovegetation data, we found that major glaciations during the Pleistocene have had a major impact upon the current genetic diversity of this species. Coalescent simulations indicate that the populations retreated to different refugia during some glacial periods in the Pleistocene, but persisted through the last glacial maximum (LGM). The most significant recent population expansion was found to have occurred before the LGM, during which palaeoclimatic data indicate that the climate was both warmer and wetter than today. In contrast, during the LGM populations may have adopted an altitudinal shift strategy in order to track changes in alpine glaciers, exemplifying a general response for montane species in the region where alpine glaciations were not large enough to cause qualitative changes in vegetation. Although analysis based on a plumage related gene showed that divergent selection may have contributed to current patterns of intra-specific diversity, demographic isolation is inferred to have played a more dominant role.

Genetic structuring and recent demographic history of red pandas (Ailurus fulgens) inferred from microsatellite and mitochondrial DNA.

Clarification of the genetic structure and population history of a species can shed light on the impacts of landscapes, historical climate change and contemporary human activities and thus enables evidence-based conservation decisions for endangered organisms. The red panda (Ailurus fulgens) is an endangered species distributing at the edge of the Qinghai-Tibetan Plateau and is currently subject to habitat loss, fragmentation and population decline, thus representing a good model to test the influences of the above-mentioned factors on a plateau edge species. We combined nine microsatellite loci and 551 bp of mitochondrial control region (mtDNA CR) to explore the genetic structure and demographic history of this species. A total of 123 individuals were sampled from 23 locations across five populations. High levels of genetic variation were identified for both mtDNA and microsatellites. Phylogeographic analyses indicated little geographic structure, suggesting historically wide gene flow. However, microsatellite-based Bayesian clustering clearly identified three groups (Qionglai-Liangshan, Xiaoxiangling and Gaoligong-Tibet). A significant isolation-by-distance pattern was detected only after removing Xiaoxiangling. For mtDNA data, there was no statistical support for a historical population expansion or contraction for the whole sample or any population except Xiaoxiangling where a signal of contraction was detected. However, Bayesian simulations of population history using microsatellite data did pinpoint population declines for Qionglai, Xiaoxiangling and Gaoligong, demonstrating significant influences of human activity on demography. The unique history of the Xiaoxiangling population plays a critical role in shaping the genetic structure of this species, and large-scale habitat loss and fragmentation is hampering gene flow among populations. The implications of our findings for the biogeography of the Qinghai-Tibetan Plateau, subspecies classification and conservation of red pandas are discussed.

Spatial patterns and conservation of genetic and phylogenetic diversity of wildlife in China.

Genetic diversity and phylogenetic diversity reflect the evolutionary potential and history of species, respectively. However, the levels and spatial patterns of genetic and phylogenetic diversity of wildlife at the regional scale have largely remained unclear. Here, we performed meta-analyses of genetic diversity in Chinese terrestrial vertebrates based on three genetic markers and investigated their phylogenetic diversity based on a dated phylogenetic tree of 2461 species. We detected strong positive spatial correlations among mitochondrial DNA-based genetic diversity, phylogenetic diversity, and species richness. Moreover, the terrestrial vertebrates harbored higher genetic and phylogenetic diversity in South China and Southwest China than in other regions. Last, climatic factors (precipitation and temperature) had significant positive effects while altitude and human population density had significant negative impacts on levels of mitochondrial DNA-based genetic diversity in most cases. Our findings will help guide national-level genetic diversity conservation plans and a post-2020 biodiversity conservation framework.