Climatic fluctuations, geographic features, and evolutionary forces: Shaping high genomic diversity and local adaptation in Muntiacus reevesi

Genetic diversity is crucial for species adaptability. Understanding the mechanisms behind its formation and maintenance is essential for effective conservation. Recent studies have demonstrated that despite experiencing severe population bottlenecks, Muntiacus reevesi retains high genetic diversity and continues its northward migration, indicative of ongoing adaptive evolution. However, our comprehension of this phenomenon remains incomplete. The objective of this study is to explore the mechanisms underlying the formation of high genetic diversity and the genomic characteristics associated with local adaptation, using M. reevesi as a case study.Southern China.We analysed resequencing data from 62 genomes and identified 29,124,081 high‐quality single‐nucleotide polymorphisms (SNPs). We used population genetics, demographic history, population differentiation, gene flow analysis software, and genotype‐environment association (GEA) models to assess the factors that have contributed to high genetic diversity and environmental adaptability in the historical climate and geographical context.The study identified that during Pleistocene climatic fluctuations, M. reevesi diverged into eastern (DB and WJW populations) and western lineages (WL, BA, and QL populations), all displayed high genetic diversity. Historically, M. reevesi maintained large effective populations, but contemporary human‐induced threats have led to a significant decline. Population differentiation models suggest distinct expansion pathways for eastern and western lineages, resulting in population admixture, with mountain corridors facilitating gene flow and maintaining high genetic diversity. Additionally, environmental‐genotype analysis revealed local adaptation in the QL‐BA population, highlighting candidate adaptive genes (ME3 and PRKG1) potentially linked to cold adaptation and foraging behaviour.This study enhances our understanding of the mechanisms behind the high genetic diversity and environmental adaptability of M. reevesi, offering insights into how bottleneck populations maintain diversity, crucial for biogeographic research and conservation strategies for similar species.

[1]  Jinzhong Fu,et al.  Impacts of Quaternary glaciation, geological history and geography on animal species history in continental East Asia: A phylogeographic review , 2023, Molecular ecology.

[2]  T. Iwasaki,et al.  The role of oceanic currents in the dispersal and connectivity of the mangrove Rhizophora mangle on the Southwest Atlantic region. , 2023, Molecular ecology resources.

[3]  U. Ramakrishnan,et al.  Gene flow drives genomic diversity in Asian Pikas distributed along the core and range‐edge habitats in the Himalayas , 2023, Ecology and evolution.

[4]  Jinzhong Fu,et al.  Whole‐genome resequencing reveals complex effects of geographical–palaeoclimatic interactions on diversification of moustache toads in East Asia , 2022, Molecular ecology.

[5]  Maxwell D. Sanderford,et al.  TimeTree 5: An Expanded Resource for Species Divergence Times , 2022, Molecular biology and evolution.

[6]  X. Zhan,et al.  Evolutionary Conservation Genomics Reveals Recent Speciation and Local Adaptation in Threatened Takins , 2022, Molecular biology and evolution.

[7]  Ran Wei,et al.  Ecological adaptation shaped the genetic structure of homoploid ferns against strong dispersal capacity , 2022, Molecular ecology.

[8]  Wen Wang,et al.  Molecular mechanisms and topological consequences of drastic chromosomal rearrangements of muntjac deer , 2021, Nature Communications.

[9]  Yu Jiang,et al.  Genome-wide scan for selective footprints and genes related to cold tolerance in Chantecler chickens , 2021, Zoological research.

[10]  J. Searle,et al.  A dynamic history of admixture from Mediterranean and Carpathian glacial refugia drives genomic diversity in the bank vole , 2021, Ecology and evolution.

[11]  D. Muzny,et al.  Comparative genomic analysis of sifakas (Propithecus) reveals selection for folivory and high heterozygosity despite endangered status , 2021, Science Advances.

[12]  William T. Harvey,et al.  Haplotype-resolved diverse human genomes and integrated analysis of structural variation , 2021, Science.

[13]  P. Orozco‐terWengel,et al.  Spatial dynamics of Chinese Muntjac related to past and future climate fluctuations , 2021, Current zoology.

[14]  Yun-Xin Fu,et al.  Stairway Plot 2: demographic history inference with folded SNP frequency spectra , 2020, Genome Biology.

[15]  F. Dai,et al.  Identification, expression, and artificial selection of silkworm epigenetic modification enzymes , 2020, BMC genomics.

[16]  M. Malinsky,et al.  Dsuite ‐ Fast D‐statistics and related admixture evidence from VCF files , 2020, Molecular ecology resources.

[17]  Xiaomin Ma,et al.  Genome-wide SNPs and indels characteristics of three chinese domestic sheep breeds from different ecoregions , 2020 .

[18]  D. Rokhsar,et al.  Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution , 2020, Communications biology.

[19]  A. Pardiñas,et al.  Recent demographic history inferred by high-resolution analysis of linkage disequilibrium. , 2020, Molecular biology and evolution.

[20]  Hang Sun,et al.  Genomic insights into adaptation to heterogeneous environments for the ancient relictual Circaeaster agrestis (Circaeasteraceae, Ranunculales). , 2020, The New phytologist.

[21]  S. Myles,et al.  Linkage Disequilibrium, Effective Population Size and Genomic Inbreeding Rates in American Mink Using Genotyping-by-Sequencing Data , 2020, Frontiers in Genetics.

[22]  S. Munné-Bosch,et al.  Global gene flow releases invasive plants from environmental constraints on genetic diversity , 2020, Proceedings of the National Academy of Sciences.

[23]  Qi Wu,et al.  Genomic evidence for two phylogenetic species and long-term population bottlenecks in red pandas , 2020, Science Advances.

[24]  K. Schmidt,et al.  Genomic patterns in the widespread Eurasian lynx shaped by Late Quaternary climatic fluctuations and anthropogenic impacts , 2020, Molecular ecology.

[25]  C. Fox,et al.  Bayesian Inference of Species Trees using Diffusion Models. , 2019, Systematic biology.

[26]  Olga Tanaseichuk,et al.  Metascape provides a biologist-oriented resource for the analysis of systems-level datasets , 2019, Nature Communications.

[27]  Abigail A. Scholer,et al.  Self-regulation and the foraging gene (PRKG1) in humans , 2019, Proceedings of the National Academy of Sciences.

[28]  O. François,et al.  LFMM 2: Fast and Accurate Inference of Gene-Environment Associations in Genome-Wide Studies , 2019, Molecular biology and evolution.

[29]  Kirk E. Lohmueller,et al.  Using Genomic Data to Infer Historic Population Dynamics of Nonmodel Organisms , 2018, Annual Review of Ecology, Evolution, and Systematics.

[30]  Aaron P. Ragsdale,et al.  Genomic inference using diffusion models and the allele frequency spectrum. , 2018, Current opinion in genetics & development.

[31]  Chi Zhang,et al.  PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files , 2018, Bioinform..

[32]  Baowei Zhang,et al.  How rivers and historical climate oscillations impact on genetic structure in Chinese Muntjac (Muntiacus reevesi)? , 2018, Diversity and Distributions.

[33]  R. Harrigan,et al.  Ecological genomics predicts climate vulnerability in an endangered southwestern songbird. , 2018, Ecology letters.

[34]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[35]  Peter D. Keightley,et al.  Inferring the Probability of the Derived vs. the Ancestral Allelic State at a Polymorphic Site , 2018, Genetics.

[36]  R. Harrigan,et al.  Genomic signals of selection predict climate-driven population declines in a migratory bird , 2018, Science.

[37]  Zhuo Li,et al.  Ten Years of Landscape Genomics: Challenges and Opportunities , 2017, Front. Plant Sci..

[38]  A. Leaché,et al.  Evaluating mechanisms of diversification in a Guineo‐Congolian tropical forest frog using demographic model selection , 2017, Molecular ecology.

[39]  F. Zhao,et al.  Population Genomics Reveals Speciation and Introgression between Brown Norway Rats and Their Sibling Species , 2017, Molecular biology and evolution.

[40]  Yun S. Song,et al.  Robust and scalable inference of population history from hundreds of unphased whole genomes , 2016, Nature Genetics.

[41]  A. M. Allen,et al.  Feeding-Related Traits Are Affected by Dosage of the foraging Gene in Drosophila melanogaster , 2016, Genetics.

[42]  H. Ellegren,et al.  Determinants of genetic diversity , 2016, Nature Reviews Genetics.

[43]  V. Friesen,et al.  Genomics of local adaptation with gene flow , 2016, Molecular ecology.

[44]  Brenna R. Forester,et al.  Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes , 2016, Molecular ecology.

[45]  Samantha R Anderson,et al.  The devil is in the details: genetic variation in introduced populations and its contributions to invasion , 2015, Molecular ecology.

[46]  Yun-Xin Fu,et al.  Exploring Population Size Changes Using SNP Frequency Spectra , 2015, Nature Genetics.

[47]  R. Nielsen,et al.  Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing , 2015, Nature Genetics.

[48]  J. Darling,et al.  How important is intraspecific genetic admixture to the success of colonising populations? , 2014, Trends in ecology & evolution.

[49]  David B. Witonsky,et al.  Admixture facilitates genetic adaptations to high altitude in Tibet , 2014, Nature Communications.

[50]  D. Silvestro,et al.  raxmlGUI: a graphical front-end for RAxML , 2012, Organisms Diversity & Evolution.

[51]  K. Wellen,et al.  Reciprocal regulation of p53 and malic enzymes modulates metabolism and senescence , 2012, Nature.

[52]  P. Andolfatto,et al.  Revisiting an Old Riddle: What Determines Genetic Diversity Levels within Species? , 2012, PLoS biology.

[53]  C. Clark,et al.  Pattern and timing of retreat of the last British-Irish Ice Sheet , 2012 .

[54]  Joseph K. Pickrell,et al.  Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data , 2012, PLoS genetics.

[55]  R. Durbin,et al.  Inference of Human Population History From Whole Genome Sequence of A Single Individual , 2011, Nature.

[56]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[57]  H. Hakonarson,et al.  ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data , 2010, Nucleic acids research.

[58]  J. Avise.  Perspective: conservation genetics enters the genomics era , 2010, Conservation Genetics.

[59]  David Reich,et al.  Population differentiation as a test for selective sweeps. , 2010, Genome research.

[60]  Richard Durbin,et al.  Fast and accurate long-read alignment with Burrows–Wheeler transform , 2010, Bioinform..

[61]  Ryan D. Hernandez,et al.  Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data , 2009, PLoS genetics.

[62]  David H. Alexander,et al.  Fast model-based estimation of ancestry in unrelated individuals. , 2009, Genome research.

[63]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[64]  O. Gaggiotti,et al.  A Genome-Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective , 2008, Genetics.

[65]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[66]  B. Goossens,et al.  Genetic viability and population history of the giant panda, putting an end to the "evolutionary dead end"? , 2007, Molecular biology and evolution.

[67]  D. Reich,et al.  Population Structure and Eigenanalysis , 2006, PLoS genetics.

[68]  R. Frankham.  Genetics and extinction , 2005 .

[69]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[70]  A. Goodridge,et al.  Effect of the CCAAT/enhancer binding protein on expression of the gene for chicken malic enzyme. , 1999, Archives of biochemistry and biophysics.

[71]  R. Greenspan,et al.  Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. , 1997, Science.

[72]  O. Gaggiotti,et al.  Population Genetic Models of Source-Sink Metapopulations , 1996, Theoretical population biology.

[73]  M. Sokolowski,et al.  Genetic localization of foraging (for): a major gene for larval behavior in Drosophila melanogaster. , 1989, Genetics.

[74]  G. A. Watterson,et al.  The homozygosity test after a change in population size. , 1986, Genetics.

[75]  E. Ball,et al.  MALIC ENZYME AND LIPOGENESIS. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Qi Wu,et al.  Giant pandas are not an evolutionary cul-de-sac: evidence from multidisciplinary research. , 2015, Molecular biology and evolution.

[77]  Sequence analysis Advance Access publication June 7, 2011 The variant call format and VCFtools , 2010 .

[78]  Zhang Baowei.  The genetic divergence and gene flow pattern of two muntjac deer ( Muntiacus reevesi) populations,Wannan and Dabie Mountains,from the effect of Yangtze River and the late Pleistocene glacial oscillations , 2010 .

[79]  F. Hofmann,et al.  Function of cGMP-dependent Protein Kinases in the Nervous System , 2005, Reviews in the neurosciences.