Population genomics reveals extensive inbreeding and purging of mutational load in wild Amur tigers

The inbreeding is a big threat for the persistence of genetic diversity in small and isolated populations of endangered species. The homozygous genome could exacerbate inbreeding depression by introducing homozygous deleterious alleles in the population. However, purging of inbreeding loads as they become homozygotes in small populations could alleviate the depression. The Amur tiger (Panthera tigris altaica) is typically exists in small population living in forests in Northeast Asia and is among the most endangered animals on the planet with great symbolic significance of conservation. By comparing with captive individuals, we revealed substantially higher and more extensive inbreeding in the wild Amur tiger population (FROH=0.51) than in captive Amur tigers (FROH=0.26). We further found much less mutational loads in wild populations when compared with captive Amur tigers. However, the frequency of loss of function and deleterious nonsynonymous mutations inside ROH regions are much lower than that in non-ROH regions in both wild and captive Amur tigers, indicating the purging may had occurred in both populations but much effective in the wild population. In addition, we found the average frequency of deleterious alleles was much lower than that of neutral alleles in the wild population, indicating that the purifying selection contributed to the purging of mutational loads in the wild Amur tigers. These findings provide valuable genome-wide evidence to support the making of future conservation plans of wild Amur tigers.

[1]  Guangyi Fan,et al.  Inbreeding depression explains killer whale population dynamics , 2023, Nature Ecology & Evolution.

[2]  Anubhab Khan.  The year of the tiger and the year of tiger genomes! , 2022, Molecular ecology resources.

[3]  Sunil Kumar Sahu,et al.  Whole-genome resequencing of Chinese pangolins reveals a population structure and provides insights into their conservation , 2022, Communications Biology.

[4]  Sunil Kumar Sahu,et al.  Genomic investigation of the Chinese alligator reveals wild‐extinct genetic diversity and genomic consequences of their continuous decline , 2022, Molecular ecology resources.

[5]  Sunil Kumar Sahu,et al.  Chromosome‐scale genomes reveal genomic consequences of inbreeding in the South China tiger: A comparative study with the Amur tiger , 2022, Molecular ecology resources.

[6]  N. Galtier,et al.  Purging of deleterious burden in the endangered Iberian lynx , 2022, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Robert M. Waterhouse,et al.  The era of reference genomes in conservation genomics. , 2022, Trends in ecology & evolution.

[8]  Z. Hou,et al.  Inbreeding status and implications for Amur tigers , 2021, Animal Conservation.

[9]  Fergal J. Martin,et al.  Population genomics of the critically endangered kākāpō , 2021, Cell genomics.

[10]  M. Holyoak,et al.  Spatial conservation prioritization for the Amur tiger in Northeast China , 2021, Ecosphere.

[11]  U. Ramakrishnan,et al.  Genomic evidence for inbreeding depression and purging of deleterious genetic variation in Indian tigers , 2021, Proceedings of the National Academy of Sciences.

[12]  B. Goossens,et al.  Genomic insights into the conservation status of the world’s last remaining Sumatran rhinoceros populations , 2021, Nature Communications.

[13]  A. Manica,et al.  African and Asian leopards are highly differentiated at the genomic level , 2021, Current Biology.

[14]  Sunil Kumar Sahu,et al.  Chromosome-scale genomes provide new insights into subspecies divergence and evolutionary characteristics of the giant panda. , 2021, Science bulletin.

[15]  Heng Li,et al.  Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm , 2021, Nature Methods.

[16]  R. Frankham,et al.  Genetic rescue: A critique of the evidence supports maximizing genetic diversity rather than minimizing the introduction of putatively harmful genetic variation , 2020 .

[17]  S. Edwards,et al.  Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant , 2020, Molecular biology and evolution.

[18]  Fei Gao,et al.  CNSA: a data repository for archiving omics data , 2020, bioRxiv.

[19]  Parice A. Brandies,et al.  The Value of Reference Genomes in the Conservation of Threatened Species , 2019, Genes.

[20]  Brendan L. O’Connell,et al.  Puma genomes from North and South America provide insights into the genomic consequences of inbreeding , 2019, Nature Communications.

[21]  T. Marquès-Bonet,et al.  Estimates of genetic load in small populations suggest extensive purging of deleterious alleles , 2019, bioRxiv.

[22]  L. Keller,et al.  Purging of highly deleterious mutations through severe bottlenecks in Alpine ibex , 2019, bioRxiv.

[23]  Guangshun Jiang,et al.  Dispersal of Amur tiger from spatial distribution and genetics within the eastern Changbai mountain of China , 2019, Ecology and evolution.

[24]  Vineet K. Sharma,et al.  Comparative analysis of corrected tiger genome provides clues to their neuronal evolution , 2019, bioRxiv.

[25]  Martin Kuhlwilm,et al.  The Genomic Footprints of the Fall and Recovery of the Crested Ibis , 2019, Current Biology.

[26]  Jianzhang Ma,et al.  Metagenomic analysis revealed the effects of goat milk feeding and breast feeding on the gut microbiome of Amur tiger cubs. , 2018, Biochemical and biophysical research communications.

[27]  J. Leeuw,et al.  Effects of extreme land fragmentation on wildlife and livestock population abundance and distribution , 2016 .

[28]  R. Wilson,et al.  A High-Resolution SNP Array-Based Linkage Map Anchors a New Domestic Cat Draft Genome Assembly and Provides Detailed Patterns of Recombination , 2016, G3: Genes, Genomes, Genetics.

[29]  James L. D. Smith,et al.  Amur tigers and leopards returning to China: direct evidence and a landscape conservation plan , 2016, Landscape Ecology.

[30]  R. Frankham.  Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. , 2015, Molecular ecology.

[31]  Peter H. Sudmant,et al.  Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding , 2015, Science.

[32]  Ellen I. Damschen,et al.  Habitat fragmentation and its lasting impact on Earth’s ecosystems , 2015, Science Advances.

[33]  D. Tallmon,et al.  Genetic rescue to the rescue. , 2015, Trends in ecology & evolution.

[34]  Yuehui Ma,et al.  Construction and Analysis of Siberian Tiger Bacterial Artificial Chromosome Library with Approximately 6.5-Fold Genome Equivalent Coverage , 2014, International journal of molecular sciences.

[35]  Yun Sung Cho,et al.  The tiger genome and comparative analysis with lion and snow leopard genomes , 2013, Nature Communications.

[36]  J. Wang,et al.  Simultaneous polyandry and heteropaternity in tiger (Panthera tigrisaltaica): Implications for conservation of genetic diversity in captive populations of felids , 2013 .

[37]  B. Curcic,et al.  THE ACTUAL RELEVANCE OF ECOLOGICAL CORRIDORS IN NATURE CONSERVATION , 2013 .

[38]  K. Nissinen,et al.  The benefits of interpopulation hybridization diminish with increasing divergence of small populations , 2012, Journal of evolutionary biology.

[39]  A. García-Dorado.  Understanding and Predicting the Fitness Decline of Shrunk Populations: Inbreeding, Purging, Mutation, and Standard Selection , 2012, Genetics.

[40]  P. Hedrick,et al.  Reevaluating and Broadening the Definition of Genetic Rescue , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[41]  R. Frankham,et al.  Assessing the benefits and risks of translocations in changing environments: a genetic perspective , 2011, Evolutionary applications.

[42]  C. Amador,et al.  The purge of genetic load through restricted panmixia in a Drosophila experiment , 2010, Journal of evolutionary biology.

[43]  N. J. Ouborg,et al.  Conservation genetics in transition to conservation genomics. , 2010, Trends in genetics : TIG.

[44]  C. Packer,et al.  Translocating lions into an inbred lion population in the Hluhluwe‐iMfolozi Park, South Africa , 2008 .

[45]  S. Khunsook,et al.  Standardized Karyotype and Idiogram of the Clouded Leopard, Neofelis nebulosa (Carnivora, Felidae) by Conventional Staining, G-banding and High-resolution Staining Technique , 2008 .

[46]  R. Frankham,et al.  Most species are not driven to extinction before genetic factors impact them. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  George R. Hughes,et al.  Wild Cats – Status Survey and Conservation Action Plan , 1998, Biodiversity & Conservation.

[48]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[49]  J. Bundgaard,et al.  Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila , 2000 .