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Home / Equine Research Bank / Mol Ecol / Genome-wide population affinities and signatures of adaptati...
Molecular ecology2024; 33(19); e17527; doi: 10.1111/mec.17527

Genome-wide population affinities and signatures of adaptation in hydruntines, sussemiones and Asian wild asses.

Abstract: The extremely rich palaeontological record of the horse family, also known as equids, has provided many examples of macroevolutionary change over the last ~55 Mya. This family is also one of the most documented at the palaeogenomic level, with hundreds of ancient genomes sequenced. While these data have advanced understanding of the domestication history of horses and donkeys, the palaeogenomic record of other equids remains limited. In this study, we have generated genome-wide data for 25 ancient equid specimens spanning over 44 Ky and spread across Anatolia, the Caucasus, Central Asia and Mongolia. Our dataset includes the genomes from two extinct species, the European wild ass, Equus hydruntinus, and the sussemione Equus ovodovi. We document, for the first time, the presence of sussemiones in Mongolia and their survival around ~3.9 Kya, a finding that should be considered when discussing the timing of the first arrival of the domestic horse in the region. We also identify strong spatial differentiation within the historical ecological range of Asian wild asses, Equus hemionus, and incomplete reproductive isolation in several groups yet considered as different species. Finally, we find common selection signatures at ANTXR2 gene in European, Asian and African wild asses. This locus, which encodes a receptor for bacterial toxins, shows no selection signal in E. ovodovi, but a 5.4-kb deletion within intron 7. Whether such genetic modifications played any role in the sussemione extinction remains unknown.
© 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.
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Publication Date: 2024-09-16 PubMed ID: 39279684DOI: 10.1111/mec.17527Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

Overview

  • This research investigates the genetic history and adaptation of extinct and extant wild equids, including hydruntines, sussemiones, and Asian wild asses, through genome-wide analysis of ancient specimens.
  • It uncovers new findings about the geographic distribution, evolutionary relationships, and genetic adaptations of these species, contributing to our understanding of their evolution and extinction.

Background

  • The horse family (equids) has a rich fossil and palaeontological record spanning approximately 55 million years, showing extensive macroevolutionary changes.
  • Equids are among the best-documented mammals in terms of palaeogenomics, with hundreds of ancient genomes sequenced, primarily focusing on the domestication histories of horses and donkeys.
  • Prior to this study, the genomic data for other equid species beyond domesticated horses and donkeys were sparse, limiting understanding of their population affinities and evolutionary history.

Study Design and Methods

  • Researchers generated genome-wide data from 25 ancient equid specimens dating back up to approximately 44,000 years (44 Ky).
  • The specimens came from various geographic regions including Anatolia, the Caucasus, Central Asia, and Mongolia, providing broad spatial coverage.
  • The dataset included genomes of two extinct species:
    • Equus hydruntinus (European wild ass, known as hydruntines)
    • Equus ovodovi (sussemione)

Key Findings

  • New Distribution and Survival Data for Sussemiones:
    • For the first time, sussemione genomes were identified in Mongolia, extending their known geographic range eastwards.
    • Evidence suggests that sussemiones survived until about 3,900 years ago around Mongolia, which overlaps with periods previously thought to signify the arrival of domestic horses in that region.
  • Population Structure and Reproductive Isolation:
    • There is strong spatial genetic differentiation among populations of the Asian wild asses (Equus hemionus) throughout their historical range.
    • The study detected incomplete reproductive isolation among groups previously classified as distinct species, highlighting the complexity of equid taxonomy and evolutionary relationships.
  • Genetic Adaptations and Selection Signatures:
    • A common signature of natural selection was detected at the ANTXR2 gene across European, Asian, and African wild asses.
    • The ANTXR2 gene encodes a receptor that binds bacterial toxins, indicating possible adaptive evolution to environmental pathogens.
    • Interestingly, the extinct sussemione (E. ovodovi) showed no such selection signal but possessed a 5.4-kilobase deletion within intron 7 of ANTXR2.
    • The functional implications of this deletion and whether it contributed to the extinction of the sussemione species remain unknown.

Significance and Implications

  • This study expands the knowledge of equid evolutionary history beyond previously focused domesticated species to include extinct wild species with new genomic data.
  • The presence of sussemiones in Mongolia later than previously thought suggests a need to reconsider the timeline for horse domestication and introduction in Central Asia.
  • Findings of incomplete reproductive isolation challenge the strict species boundaries of Asian wild asses, implying gene flow among groups with conservation and evolutionary implications.
  • Identification of shared and unique genetic adaptations, especially involving immunity-related genes like ANTXR2, opens avenues for exploring how wild equids adapted to their environments and pathogens.
  • Understanding genetic changes linked to extinction events in extinct species like the sussemione may help unravel factors contributing to their demise, relevant for conserving extant equid species.

Cite This Article

APA
(2024). Genome-wide population affinities and signatures of adaptation in hydruntines, sussemiones and Asian wild asses. Mol Ecol, 33(19), e17527. https://doi.org/10.1111/mec.17527

Publication

Molecular ecology
ISSN: 1365-294X
NlmUniqueID: 9214478
Country: England
Language: English
Volume: 33
Issue: 19
Pages: e17527

Researcher Affiliations

MeSH Terms

  • Animals
  • Equidae / genetics
  • Genetics, Population
  • Mongolia
  • Genome / genetics
  • Phylogeny
  • Fossils
  • Horses / genetics
  • Adaptation, Physiological / genetics

Grant Funding

  • 101027750 / European Union's Horizon 2020 research and innovation programme
  • 101062645 / European Union's Horizon 2020 research and innovation programme
  • Agricultural Science and Technology Innovation Program (ASTIP-05)
  • CNRS and University Paul Sabatier (AnimalFarm IRP)
  • Spanish Ministerio de Educación, Cultura y Deporte (Archaeological Projects Abroad 2017)
  • Wroclaw Centre of Biotechnology programme ('The Leading National Research Center [KNOW]')
  • 681605 / HORIZON EUROPE European Research Council
  • 834616 / HORIZON EUROPE European Research Council
  • 101071707 / HORIZON EUROPE European Research Council
  • ANR-10-INBS-09 / Agence Nationale pour la Recherche
  • 19-78-10053 / Russian Science Foundation
  • 22-18-00194 / Russian Science Foundation

References

This article includes 70 references
  1. Ahrens E, Stranzinger G. Comparative chromosomal studies of E. Caballus (ECA) and E. Przewalskii (EPR) in a female F1 hybrid. Journal of Animal Breeding and Genetics 122 Suppl 1, 97–102.
    doi: 10.1111/j.1439‐0388.2005.00494.xgoogle scholar: lookup
  2. Alexander DH, Novembre J, Lange K. Fast model‐based estimation of ancestry in unrelated individuals. Genome Research 19(9), 1655–1664.
    doi: 10.1101/gr.094052.109google scholar: lookup
  3. Banks DJ, Barnajian M, Maldonado‐Arocho FJ, Sanchez AM, Bradley KA. Anthrax toxin receptor 2 mediates bacillus anthracis killing of macrophages following spore challenge. Cellular Microbiology 7(8), 1173–1185.
    doi: 10.1111/j.1462‐5822.2005.00545.xgoogle scholar: lookup
  4. Bennett EA, Champlot S, Peters J, Arbuckle BS, Guimaraes S, Pruvost M, Bar‐David S, Davis SJM, Gautier M, Kaczensky P, Kuehn R, Mashkour M, Morales‐Muñiz A, Pucher E, Tournepiche JF, Uerpmann HP, Bălăşescu A, Germonpré M, Gündem CY, Geigl EM. Taming the late quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA. PLoS One 12(4), e0174216.
    doi: 10.1371/journal.pone.0174216google scholar: lookup
  5. Cai D, Zhu S, Gong M, Zhang N, Wen J, Liang Q, Sun W, Shao X, Guo Y, Cai Y, Zheng Z, Zhang W, Hu S, Wang X, Tian H, Li Y, Liu W, Yang M, Yang J, Jiang Y. Radiocarbon and genomic evidence for the survival of Equus Sussemionus until the late Holocene. eLife 11, e73346.
    doi: 10.7554/elife.73346google scholar: lookup
  6. Catalano G, Modi A, Mangano G, Sineo L, Lari M, Bonfiglio L. A mitogenome sequence of an Equus hydruntinus specimen from late quaternary site of san Teodoro cave (Sicily, Italy). Quaternary Science Reviews 236, 106280.
    doi: 10.1016/j.quascirev.2020.106280google scholar: lookup
  7. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second‐generation PLINK: Rising to the challenge of larger and richer datasets. GigaScience 4(1), 7.
    doi: 10.1186/s13742‐015‐0047‐8google scholar: lookup
  8. Cheng JY, Stern AJ, Racimo F, Nielsen R. Detecting selection in multiple populations by modeling ancestral admixture components. Molecular Biology and Evolution 39(1), msab294.
    doi: 10.1093/molbev/msab294google scholar: lookup
  9. Crees JJ, Turvey ST. Holocene extinction dynamics of Equus hydruntinus, a late‐surviving European megafaunal mammal. Quaternary Science Reviews 91, 16–29.
    doi: 10.1016/j.quascirev.2014.03.003google scholar: lookup
  10. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R. The variant call format and VCFtools. Bioinformatics 27(15), 2156–2158.
    doi: 10.1093/bioinformatics/btr330google scholar: lookup
  11. Der Sarkissian C, Ermini L, Schubert M, Yang MA, Librado P, Fumagalli M, Jónsson H, Bar‐Gal GK, Albrechtsen A, Vieira FG, Petersen B, Ginolhac A, Seguin‐Orlando A, Magnussen K, Fages A, Gamba C, Lorente‐Galdos B, Polani S, Steiner C, Orlando L. Evolutionary genomics and conservation of the endangered Przewalski's horse. Current Biology 25(19), 2577–2583.
    doi: 10.1016/j.cub.2015.08.032google scholar: lookup
  12. Dickson CC. Whole genome sequencing reveals genes and pathways associated with anthrax survivorship in plains zebra. .
  13. Druzhkova AS, Makunin AI, Vorobieva NV, Vasiliev SK, Ovodov ND, Shunkov MV, Trifonov VA, Graphodatsky AS. Complete mitochondrial genome of an extinct Equus (Sussemionus) ovodovi specimen from Denisova cave (Altai, Russia). Mitochondrial DNA Part B Resources 2(1), 79–81.
    doi: 10.1080/23802359.2017.1285209google scholar: lookup
  14. Fages A, Hanghøj K, Khan N, Gaunitz C, Seguin‐Orlando A, Leonardi M, Constantz CM, Gamba C, Al‐Rasheid KA, Albizuri S. Tracking five millennia of horse management with extensive ancient genome time series. Cell 177, 1419–1435.e31.
  15. Fitak RR. OptM: Estimating the optimal number of migration edges on population trees using Treemix. Biology Methods & Protocols 6(1), bpab017.
    doi: 10.1093/biomethods/bpab017google scholar: lookup
  16. Gaunitz C, Fages A, Hanghøj K, Albrechtsen A, Khan N, Schubert M, Bignon‐Lau O. Ancient genomes revisit the ancestry of domestic and Przewalski's horses. Science 360(6384), 111–114.
    doi: 10.1126/science.aao3297google scholar: lookup
  17. Guo Q, Ullah I, Zheng LJ, Gao XQ, Liu CY, Zheng HD, Fan LH, Deng L. Intelligent self‐control of carbon metabolic flux in SecY‐engineered Escherichia coli for xylitol biosynthesis from xylose‐glucose mixtures. Biotechnology and Bioengineering 119(2), 388–398.
    doi: 10.1002/bit.28002google scholar: lookup
  18. Guo S, Chunyu L, Ouyang S, Wang X, Liao A, Yuan S. GOLGA4, A Golgi matrix protein, is dispensable for spermatogenesis and male fertility in mice. Biochemical and Biophysical Research Communications 529(3), 642–646.
    doi: 10.1016/j.bbrc.2020.05.170google scholar: lookup
  19. Houle J‐L, Seitsonen O, Égüez N, Broderick LG, García‐Granero JJ, Bayarsaikhan J. Resilient herders: A deeply stratified multiperiod habitation site in northwestern Mongolia. Archaeological Research in Asia 30, 100371.
    doi: 10.1016/j.ara.2022.100371google scholar: lookup
  20. Jónsson H, Ginolhac A, Schubert M, Johnson PL, Orlando L. mapDamage2. 0: Fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29(13), 1682–1684.
    doi: 10.1093/bioinformatics/btt193google scholar: lookup
  21. Jónsson H, Schubert M, Seguin‐Orlando A, Ginolhac A, Petersen L, Fumagalli M, Albrechtsen A, Petersen B, Korneliussen TS, Vilstrup JT, Lear T, Myka JL, Lundquist J, Miller DC, Alfarhan AH, Alquraishi SA, Al‐Rasheid KA, Stagegaard J, Strauss G, Orlando L. Speciation with gene flow in equids despite extensive chromosomal plasticity. Proceedings of the National Academy of Sciences 111(52), 18655–18660.
    doi: 10.1073/pnas.1412627111google scholar: lookup
  22. Kaczensky P, Lkhagvasuren B, Pereladova O, Hemami M, Bouskila A. Equus hemionus (amended version of 2015 assessment). The IUCN Red List of Threatened Species e. T7951A166520460.
    doi: 10.2305/iucn.uk.2020‐1.rlts.t7951a166520460.engoogle scholar: lookup
  23. Karlowicz A, Dubiel AB, Czerwinska J, Bledea A, Purzycki P, Grzelewska M, McAuley RJ, Szczesny RJ, Brzuska G, Krol E, Szczesny B, Szymanski MR. In vitro reconstitution reveals a key role of human mitochondrial EXOG in RNA primer processing. Nucleic Acids Research 50(14), 7991–8007.
    doi: 10.1093/nar/gkac581google scholar: lookup
  24. Lefort V, Desper R, Gascuel O. FastME 2.0: A comprehensive, accurate, and fast distance‐based phylogeny inference program. Molecular Biology and Evolution 32(10), 2798–2800.
    doi: 10.1093/molbev/msv150google scholar: lookup
  25. Leviyang S, Hamilton MB. Properties of weir and Cockerham's Fst estimators and associated bootstrap confidence intervals. Theoretical Population Biology 79(1–2), 39–52.
    doi: 10.1016/j.tpb.2010.11.001google scholar: lookup
  26. Li W, Yin L, Shen C, Hu K, Ge J, Sun A. SCN5A variants: Association with cardiac disorders. Frontiers in Physiology 9, 1372.
    doi: 10.3389/fphys.2018.01372google scholar: lookup
  27. Librado P, Khan N, Fages A, Kusliy MA, Suchan T, Tonasso‐Calvière L, Perdereau A, Aury JM, Gaunitz C, Chauvey L, Seguin‐Orlando A, Der Sarkissian C, Southon J, Shapiro B, Tishkin AA, Kovalev AA, Alquraishi S, Alfarhan AH, Al‐Rasheid KAS, Orlando L. The origins and spread of domestic horses from the Western Eurasian steppes. Nature 598(7882), 634–640.
    doi: 10.1038/s41586‐021‐04018‐9google scholar: lookup
  28. Librado P, Tressières G, Chauvey L, Fages A, Khan N, Schiavinato S, Calvière‐Tonasso L, Kusliy MA, Gaunitz C, Liu X, Wagner S, Der Sarkissian C, Seguin‐Orlando A, Perdereau A, Aury JM, Southon J, Shapiro B, Bouchez O, Donnadieu C, Orlando L. Widespread horse‐based mobility arose around 2200 BCE in Eurasia. Nature 631, 819–825.
  29. MacFadden BJ. Fossil horses from “eohippus”(Hyracotherium) to Equus: Scaling, Cope's law, and the evolution of body size. Paleobiology 12(4), 355–369.
    doi: 10.1017/s0094837300003109google scholar: lookup
  30. Malinsky M, Matschiner M, Svardal H. Dsuite—fast D‐statistics and related admixture evidence from VCF files. Molecular Ecology Resources 21(2), 584–595.
    doi: 10.1111/1755‐0998.13265google scholar: lookup
  31. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. The genome analysis toolkit: A MapReduce framework for analyzing next‐generation DNA sequencing data. Genome Research 20(9), 1297–1303.
    doi: 10.1101/gr.107524.110google scholar: lookup
  32. Milanesi M, Capomaccio S, Vajana E, Bomba L, Garcia JF, Ajmone‐Marsan P, Colli L. BITE: An R package for biodiversity analyses. bioRxiv 181610.
    doi: 10.1101/181610google scholar: lookup
  33. Musilova P, Kubickova S, Horin P, Vodicka R, Rubes J. Karyotypic relationships in Asiatic asses (kulan and kiang) as defined using horse chromosome arm‐specific and region‐specific probes. Chromosome Research 17(6), 783–790.
    doi: 10.1007/s10577‐009‐9069‐3google scholar: lookup
  34. Nguyen L‐T, Schmidt HA, Von Haeseler A, Minh BQ. IQ‐TREE: A fast and effective stochastic algorithm for estimating maximum‐likelihood phylogenies. Molecular Biology and Evolution 32(1), 268–274.
    doi: 10.1093/molbev/msu300google scholar: lookup
  35. Olsen S, Zeder M. 17. Early horse domestication on the eurasian steppe. Documenting domestication: New genetic and archaeological paradigms pp. 245–270.
    doi: 10.1525/9780520932425‐020google scholar: lookup
  36. Orlando L. Equids. Current Biology 25(20), R973–R978.
    doi: 10.1016/j.cub.2015.09.005google scholar: lookup
  37. Orlando L, Allaby R, Skoglund P, Der Sarkissian C, Stockhammer PW, Ávila‐Arcos MC, Fu Q, Krause J, Willerslev E, Stone AC, Warinner C. Ancient DNA analysis. Nature Reviews Methods Primers 1(1), 14.
    doi: 10.1038/s43586‐020‐00011‐0google scholar: lookup
  38. Orlando L, Cooper A. Using ancient DNA to understand evolutionary and ecological processes. Annual Review of Ecology, Evolution, and Systematics 45, 573–598.
    doi: 10.1146/annurev‐ecolsys‐120213‐091712google scholar: lookup
  39. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early middle Pleistocene horse. Nature 499(7456), 74–78.
    doi: 10.1038/nature12323google scholar: lookup
  40. Orlando L, Mashkour M, Burke A, Douady CJ, Eisenmann V, Haenni C. Geographic distribution of an extinct equid (Equus hydruntinus: Mammalia, Equidae) revealed by morphological and genetical analyses of fossils. Molecular Ecology 15(8), 2083–2093.
    doi: 10.1111/j.1365‐294x.2006.02922.xgoogle scholar: lookup
  41. Orlando L, Metcalf JL, Alberdi MT, Telles‐Antunes M, Bonjean D, Otte M, Morello F. Revising the recent evolutionary history of equids using ancient DNA. Proceedings of the National Academy of Sciences 106(51), 21754–21759.
    doi: 10.1073/pnas.0903672106google scholar: lookup
  42. Owen‐Smith N. Contrasts in the large herbivore faunas of the southern continents in the late Pleistocene and the ecological implications for human origins. Journal of Biogeography 40(7), 1215–1224.
    doi: 10.1111/jbi.12100google scholar: lookup
  43. Özkan M, Gürün K, Yüncü E, Vural KB, Atağ G, Akbaba A, Fidan FR, Sağlıcan E, Altınışık EN, Koptekin D. The first complete genome of the extinct European wild ass (Equus hemionus hydruntinus). Molecular Ecology 33, e17440.
    doi: 10.1111/mec.17440google scholar: lookup
  44. Pickrell J, Pritchard J. Inference of population splits and mixtures from genome‐wide allele frequency data. PLoS Genetics 8(11), e1002967.
    doi: 10.1371/journal.pgen.1002967google scholar: lookup
  45. Popović D, Molak M, Ziółkowski M, Vranich A, Sobczyk M, Vidaurre DU, Agresti G, Skrzypczak M, Ginalski K, Lamnidis TC, Nakatsuka N, Mallick S, Baca M. Ancient genomes reveal long‐range influence of the pre‐Columbian culture and site of Tiwanaku. Science Advances 7(39), eabg7261.
    doi: 10.1126/sciadv.abg7261google scholar: lookup
  46. Poullet M, Orlando L. Assessing DNA sequence alignment methods for characterizing ancient genomes and methylomes. Frontiers in Ecology and Evolution 8, 105.
    doi: 10.3389/fevo.2020.00105google scholar: lookup
  47. Reimer PJ, Austin WE, Bard E, Bayliss A, Blackwell PG, Ramsey CB, Friedrich M, Grootes PM. The IntCal20 northern hemisphere radiocarbon age calibration curve (0–55 cal kBP). Radiocarbon 62(4), 725–757.
    doi: 10.1017/rdc.2020.41google scholar: lookup
  48. Rocha J, Silva P, Santos N, Nakamura M, Afonso S, Qninba A, Boratynski Z, Sudmant PH, Brito JC, Nielsen R, Godinho R. North African fox genomes show signatures of repeated introgression and adaptation to life in deserts. Nature Ecology & Evolution 1–20, 1267–1286.
    doi: 10.1038/s41559‐023‐02094‐wgoogle scholar: lookup
  49. Rogers RL, Slatkin M. Excess of genomic defects in a woolly mammoth on Wrangel Island. PLoS Genetics 13(3), e1006601.
    doi: 10.1371/journal.pgen.1006601google scholar: lookup
  50. Rosenbom S, Costa V, Chen S, Khalatbari L, Yusefi GH, Abdukadir A, Yangzom C, Kebede F, Teclai R, Yohannes H, Hagos F, Moehlman PD, Beja‐Pereira A. Reassessing the evolutionary history of ass‐like equids: Insights from patterns of genetic variation in contemporary extant populations. Molecular Phylogenetics and Evolution 85, 88–96.
    doi: 10.1016/j.ympev.2015.01.005google scholar: lookup
  51. Schubert M, Ermini L, Sarkissian CD, Jónsson H, Ginolhac A, Schaefer R, Martin MD, Fernández R, Kircher M, McCue M, Willerslev E, Orlando L. Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX. Nature Protocols 9(5), 1056–1082.
    doi: 10.1038/nprot.2014.063google scholar: lookup
  52. Schubert M, Lindgreen S, Orlando L. AdapterRemoval v2: Rapid adapter trimming, identification, and read merging. BMC Research Notes 9(1), 1–7.
    doi: 10.1186/s13104‐016‐1900‐2google scholar: lookup
  53. Schubert M, Mashkour M, Gaunitz C, Fages A, Seguin‐Orlando A, Sheikhi S, Alfarhan AH, Alquraishi SA, Al‐Rasheid KA, Chuang R, Ermini L. Zonkey: A simple, accurate and sensitive pipeline to genetically identify equine F1‐hybrids in archaeological assemblages. Journal of Archaeological Science 78, 147–157.
    doi: 10.1016/j.jas.2016.12.005google scholar: lookup
  54. Scott A, Reinhold S, Hermes T, Kalmykov AA, Belinskiy A, Buzhilova A, Berezina N, Kantorovich AR, Maslov VE, Guliyev F, Lyonnet B, Gasimov P, Jalilov B, Eminli J, Iskandarov E, Hammer E, Nugent SE, Hagan R, Majander K, Warinner C. Emergence and intensification of dairying in the Caucasus and Eurasian steppes. Nature Ecology & Evolution 6(6), 813–822.
    doi: 10.1038/s41559‐022‐01701‐6google scholar: lookup
  55. Sinha R, Siddiqui TJ, Padmanabhan N, Wallin J, Zhang C, Karimi B, Rieke F, Craig AM, Wong RO, Hoon M. LRRTM4: A novel regulator of presynaptic inhibition and ribbon synapse arrangements of retinal bipolar cells. Neuron 105(6), 1007–1017.e1005.
    doi: 10.1016/j.neuron.2019.12.028google scholar: lookup
  56. Strani F, DeMiguel D. The role of climate change in the extinction of the last wild equids of Europe: Palaeoecology of Equus ferus and Equus hydruntinus during the last glacial period. Palaeogeography, Palaeoclimatology, Palaeoecology 620, 111564.
    doi: 10.1016/j.palaeo.2023.111564google scholar: lookup
  57. Swan J, Szabó Z, Peters J, Kummu O, Kemppi A, Rahtu‐Korpela L, Konzack A, Hakkola J, Pasternack A, Ritvos O, Kerkelä R, Magga J. Inhibition of activin receptor 2 signalling ameliorates metabolic dysfunction‐associated steatotic liver disease in western diet/L‐NAME induced cardiometabolic disease. Biomedicine & Pharmacotherapy 175, 116683.
    doi: 10.1016/j.biopha.2024.116683google scholar: lookup
  58. Taylor W, Shnaider S, Abdykanova A, Fages A, Welker F, Irmer F, Seguin‐Orlando A, Khan N, Douka K, Kolobova K, Orlando L, Krivoshapkin A, Boivin N. Early pastoral economies along the ancient silk road: Biomolecular evidence from the Alay Valley Kyrgyzstan. PLoS One 13(10), e0205646.
    doi: 10.1371/journal.pone.0205646google scholar: lookup
  59. Taylor WTT, Jargalan B, Lowry KB, Clark J, Tuvshinjargal T, Bayarsaikhan J. A Bayesian chronology for early domestic horse use in the eastern steppe. Journal of Archaeological Science 81, 49–58.
    doi: 10.1016/j.jas.2017.03.006google scholar: lookup
  60. Todd ET, Tonasso‐Calvière L, Chauvey L, Schiavinato S, Fages A, Seguin‐Orlando A, Clavel P, Khan N, Pérez Pardal L, Patterson Rosa L, Librado P, Ringbauer H, Verdugo M, Southon J, Aury JM, Perdereau A, Vila E, Marzullo M, Prato O, Orlando L. The genomic history and global expansion of domestic donkeys. Science 377(6611), 1172–1180.
    doi: 10.1126/science.abo3503google scholar: lookup
  61. van Asperen EN, Stefaniak K, Proskurnyak I, Ridush B. Equids from Emine‐Bair‐Khosar cave (Crimea, Ukraine): co‐occurrence of the stenonid Equus hydruntinus and the caballoid E. Ferus latipes based on skull and postcranial remains. Palaeontologia Electronica 15(1), 1–28.
    doi: 10.26879/280google scholar: lookup
  62. van der Valk T, Dehasque M, Chacón‐Duque JC, Oskolkov N, Vartanyan S, Heintzman PD, Pečnerová P, Díez‐Del‐Molino D, Dalén L. Evolutionary consequences of genomic deletions and insertions in the woolly mammoth genome. Iscience 25(8), 104826.
    doi: 10.1016/j.isci.2022.104826google scholar: lookup
  63. Vasiliev S. Large mammal fauna from the Pleistocene deposits of Chagyrskaya cave northwestern Altai (based on 2007–2011 excavations). Archaeology, Ethnology and Anthropology of Eurasia 41(1), 28–44.
    doi: 10.1016/j.aeae.2013.07.003google scholar: lookup
  64. Ventresca Miller AR, Wilkin S, Hendy J, Turbat T, Batsukh D, Bayarkhuu N, Giscard PH, Bemmann J, Bayarsaikhan J, Miller BK, Clark J, Roberts P, Boivin N. The spread of herds and horses into the Altai: How livestock and dairying drove social complexity in Mongolia. PLoS One 17(5), e0265775.
    doi: 10.1371/journal.pone.0265775google scholar: lookup
  65. Vershinina AO, Heintzman PD, Froese DG, Zazula G, Cassatt‐Johnstone M, Dalén L, Der Sarkissian C, Dunn SG, Ermini L, Gamba C, Groves P, Kapp JD, Mann DH, Seguin‐Orlando A, Southon J, Stiller M, Wooller MJ, Baryshnikov G, Gimranov D, Shapiro B. Ancient horse genomes reveal the timing and extent of dispersals across the Bering land bridge. Molecular Ecology 30(23), 6144–6161.
    doi: 10.1111/mec.15977google scholar: lookup
  66. Vilstrup JT, Seguin‐Orlando A, Stiller M, Ginolhac A, Raghavan M, Nielsen SC, Weinstock J, Froese D, Vasiliev SK, Ovodov ND, Clary J, Helgen KM, Fleischer RC, Cooper A, Shapiro B, Orlando L. Mitochondrial phylogenomics of modern and ancient equids. PLoS One 8(2), e55950.
    doi: 10.1371/journal.pone.0055950google scholar: lookup
  67. Wade C, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Zody MC. Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326(5954), 865–867.
    doi: 10.1126/science.1178158google scholar: lookup
  68. Wang Y, Pedersen MW, Alsos IG, De Sanctis B, Racimo F, Prohaska A, Coissac E, Owens HL, Merkel MKF, Fernandez‐Guerra A, Rouillard A, Lammers Y, Alberti A, Denoeud F, Money D, Ruter AH, McColl H, Larsen NK, Cherezova AA, Willerslev E. Late quaternary dynamics of Arctic biota from ancient environmental genomics. Nature 600(7887), 86–92.
    doi: 10.1038/s41586‐021‐04016‐xgoogle scholar: lookup
  69. Wilkin S, Ventresca Miller A, Fernandes R, Spengler R, Taylor WTT, Brown DR, Reich D, Kennett DJ, Culleton BJ, Kunz L, Fortes C, Kitova A, Kuznetsov P, Epimakhov A, Zaibert VF, Outram AK, Kitov E, Khokhlov A, Anthony D, Boivin N. Dairying enabled early bronze age yamnaya steppe expansions. Nature 598(7882), 629–633.
    doi: 10.1038/s41586‐021‐03798‐4google scholar: lookup
  70. Xu Y, Zhang J, Zhang Q, Xu H, Liu L. Long non‐coding RNA HOXA11‐AS modulates proliferation, apoptosis, metastasis and EMT in cutaneous melanoma cells partly via miR‐152‐3p/ITGA9 Axis. Cancer Management and Research 13, 925–939.
    doi: 10.2147/cmar.s281920google scholar: lookup

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