African Suid Genomes Provide Insights into the Local Adaptation to Diverse African Environments.

Hai-Bing Xie, Chen Yan, Adeniyi C Adeola, Kun Wang, Cui-Ping Huang, Ming-Min Xu, Qiang Qiu, Xue Yin, Chen-Yu Fan, Yun-Fei Ma, Ting-Ting Yin, Yun Gao, Jia-Kun Deng, Agboola O Okeyoyin, Olufunke O Oluwole, Oladipo Omotosho, Victor M O Okoro, Ofelia G Omitogun, Philip M Dawuda, Sunday C Olaogun, Lotanna M Nneji, Adeola O Ayoola, Oscar J Sanke, Pam D Luka, Edward Okoth, Isaac Lekolool, Dominic Mijele, Richard P Bishop, Jianlin Han, Wen Wang, Min-Sheng Peng, Ya-Ping Zhang
Author Information
  1. Hai-Bing Xie: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  2. Chen Yan: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  3. Adeniyi C Adeola: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  4. Kun Wang: School of Ecology and Environment, Northwestern Polytechnical University, Xi'an 710129, China. ORCID
  5. Cui-Ping Huang: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  6. Ming-Min Xu: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  7. Qiang Qiu: School of Ecology and Environment, Northwestern Polytechnical University, Xi'an 710129, China.
  8. Xue Yin: State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, School of Life Sciences, Yunnan University, Kunming 650091, China.
  9. Chen-Yu Fan: State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, School of Life Sciences, Yunnan University, Kunming 650091, China.
  10. Yun-Fei Ma: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  11. Ting-Ting Yin: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  12. Yun Gao: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  13. Jia-Kun Deng: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  14. Agboola O Okeyoyin: National Park Service Headquarter, Federal Capital Territory, Abuja 900108, Nigeria.
  15. Olufunke O Oluwole: Institute of Agricultural Research and Training, Obafemi Awolowo University, Ibadan, Nigeria.
  16. Oladipo Omotosho: Department of Veterinary Medicine, University of Ibadan, Ibadan 200005, Nigeria.
  17. Victor M O Okoro: Department of Animal Science and Technology, School of Agriculture and Agricultural Technology, Federal University of Technology, Owerri 460114, Nigeria. ORCID
  18. Ofelia G Omitogun: Department of Animal Sciences, Obafemi Awolowo University, Ile-Ife 220282, Nigeria.
  19. Philip M Dawuda: Department of Veterinary Surgery and Theriogenology, College of Veterinary Medicine, University of Agriculture Makurdi, Makurdi 970001, Nigeria.
  20. Sunday C Olaogun: Department of Veterinary Medicine, University of Ibadan, Ibadan 200005, Nigeria.
  21. Lotanna M Nneji: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  22. Adeola O Ayoola: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  23. Oscar J Sanke: Taraba State Ministry of Agriculture and Natural Resources, Jalingo 660213, Nigeria.
  24. Pam D Luka: National Veterinary Research Institute, Vom 930103, Nigeria.
  25. Edward Okoth: International Livestock Research Institute (ILRI), Nairobi 00100, Kenya.
  26. Isaac Lekolool: Kenya Wildlife Services, Nairobi 00100, Kenya.
  27. Dominic Mijele: Kenya Wildlife Services, Nairobi 00100, Kenya.
  28. Richard P Bishop: International Livestock Research Institute (ILRI), Nairobi 00100, Kenya.
  29. Jianlin Han: International Livestock Research Institute (ILRI), Nairobi 00100, Kenya.
  30. Wen Wang: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  31. Min-Sheng Peng: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
  32. Ya-Ping Zhang: State Key Laboratory of Genetic Resources and Evolution & Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China. ORCID

Abstract

African wild suids consist of several endemic species that represent ancient members of the family Suidae and have colonized diverse habitats on the African continent. However, limited genomic resources for African wild suids hinder our understanding of their evolution and genetic diversity. In this study, we assembled high-quality genomes of a common warthog (Phacochoerus africanus), a red river hog (Potamochoerus porcus), as well as an East Asian Diannan small-ear pig (Sus scrofa). Phylogenetic analysis showed that common warthog and red river hog diverged from their common ancestor around the Miocene/Pliocene boundary, putatively predating their entry into Africa. We detected species-specific selective signals associated with sensory perception and interferon signaling pathways in common warthog and red river hog, respectively, which contributed to their local adaptation to savannah and tropical rainforest environments, respectively. The structural variation and evolving signals in genes involved in T-cell immunity, viral infection, and lymphoid development were identified in their ancestral lineage. Our results provide new insights into the evolutionary histories and divergent genetic adaptations of African suids.

Keywords

References

Science. 2009 Aug 7;325(5941):710-4 [PMID: 19661421]
J Med Entomol. 2013 May;50(3):479-84 [PMID: 23802441]
Nucleic Acids Res. 2019 Jan 8;47(D1):D427-D432 [PMID: 30357350]
Cell Host Microbe. 2013 Aug 14;14(2):136-47 [PMID: 23954153]
PLoS One. 2015 Apr 20;10(4):e0124069 [PMID: 25894218]
Nat Rev Immunol. 2008 Jul;8(7):559-68 [PMID: 18575461]
Anim Reprod Sci. 2006 Jan;91(1-2):155-71 [PMID: 15876499]
Nature. 2012 Mar 11;483(7390):465-9 [PMID: 22407321]
Int J Parasitol Parasites Wildl. 2021 Dec 01;17:14-19 [PMID: 34934619]
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W435-9 [PMID: 16845043]
Curr Protoc Bioinformatics. 2009 Mar;Chapter 4:Unit 4.10 [PMID: 19274634]
Mol Ecol Resour. 2019 Jul;19(4):944-956 [PMID: 30735609]
Gigascience. 2017 Dec 1;6(12):1-5 [PMID: 29099922]
Brief Bioinform. 2002 Sep;3(3):275-84 [PMID: 12230036]
Curr Biol. 2019 Sep 9;29(17):2926-2935.e4 [PMID: 31402299]
Bioinformatics. 2014 Oct 15;30(20):2843-51 [PMID: 24974202]
Nat Methods. 2012 Jul 30;9(8):772 [PMID: 22847109]
Nat Rev Neurosci. 2014 Jul;15(7):443-54 [PMID: 24917305]
Nucleic Acids Res. 2022 Jan 7;50(D1):D27-D38 [PMID: 34718731]
Neuron. 2012 Aug 23;75(4):648-62 [PMID: 22920256]
Mol Biol Evol. 2021 Mar 9;38(3):876-890 [PMID: 32986826]
PLoS Genet. 2019 Nov 25;15(11):e1008485 [PMID: 31765391]
Genome Biol. 2015 Apr 08;16:72 [PMID: 25886137]
J Cell Sci. 2015 Nov 15;128(22):4039-45 [PMID: 26574505]
Cell Mol Life Sci. 2021 Dec;78(23):7427-7434 [PMID: 34714359]
Sci Rep. 2020 Jun 2;10(1):8951 [PMID: 32488046]
Annu Rev Anim Biosci. 2015;3:139-67 [PMID: 25493538]
Science. 2013 Mar 29;339(6127):1578-82 [PMID: 23413192]
Sci Adv. 2021 Mar 17;7(12): [PMID: 33731352]
Genome Res. 2005 Aug;15(8):1034-50 [PMID: 16024819]
Trends Ecol Evol. 2006 Oct;21(10):569-75 [PMID: 16820244]
Bioinformatics. 2014 May 1;30(9):1312-3 [PMID: 24451623]
Genome Res. 2004 Apr;14(4):708-15 [PMID: 15060014]
Bioinformatics. 2005 Jun;21 Suppl 1:i351-8 [PMID: 15961478]
Mol Biol Evol. 2022 Jul 2;39(7): [PMID: 35779009]
Science. 2019 Jun 21;364(6446): [PMID: 31221828]
Gigascience. 2020 Jun 1;9(6): [PMID: 32543654]
Mol Ecol Resour. 2019 Jul;19(4):1015-1026 [PMID: 30972949]
PLoS Biol. 2010 Dec 21;8(12):e1000564 [PMID: 21203580]
PLoS One. 2013;8(4):e59831 [PMID: 23573212]
Arch Virol. 2003 Dec;148(12):2307-23 [PMID: 14648288]
Genet Sel Evol. 2016 Mar 29;48:23 [PMID: 27025270]
Science. 2018 Jun 8;360(6393): [PMID: 29880660]
Nat Genet. 2000 May;25(1):25-9 [PMID: 10802651]
Mol Biol Evol. 2015 Mar;32(3):600-12 [PMID: 25534031]
Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
Ecohealth. 2009 Jun;6(2):296-310 [PMID: 19915917]
Cytogenet Cell Genet. 1998;83(1-2):139-46 [PMID: 9925951]
Genome Res. 2017 May;27(5):737-746 [PMID: 28100585]
Heredity (Edinb). 2003 Oct;91(4):361-72 [PMID: 14512951]
Genome Res. 2011 Mar;21(3):487-93 [PMID: 21209072]
Nucleic Acids Res. 1999 Jan 15;27(2):573-80 [PMID: 9862982]
Nucleic Acids Res. 2019 Jan 8;47(D1):D351-D360 [PMID: 30398656]
J Evol Biol. 2007 May;20(3):965-70 [PMID: 17465907]
Bioinformatics. 2015 Oct 1;31(19):3210-2 [PMID: 26059717]
Science. 2016 Oct 7;354(6308):54-59 [PMID: 27846491]
Genet Sel Evol. 2020 Feb 7;52(1):4 [PMID: 32033531]
J Hum Evol. 2018 Aug;121:1-11 [PMID: 29685749]
Mol Biol Evol. 2004 Mar;21(3):468-88 [PMID: 14660683]
Brief Bioinform. 2011 Jan;12(1):41-51 [PMID: 21278375]
Nucleic Acids Res. 2017 Jan 4;45(D1):D353-D361 [PMID: 27899662]
Methods Mol Biol. 2009;537:243-61 [PMID: 19378148]
Nat Rev Microbiol. 2018 Jul;16(7):423-439 [PMID: 29769653]
Virology. 2017 Jan 15;501:102-106 [PMID: 27898335]
Mol Biol Evol. 2021 Jan 23;38(2):531-544 [PMID: 32960966]
PLoS Genet. 2009 Oct;5(10):e1000698 [PMID: 19851448]
BMC Biol. 2020 Oct 8;18(1):136 [PMID: 33032594]
PLoS One. 2013;8(2):e56235 [PMID: 23437100]
Mol Biol Evol. 2022 Jun 2;39(6): [PMID: 35642310]
Syst Biol. 2003 Oct;52(5):696-704 [PMID: 14530136]
PLoS Pathog. 2015 Oct 27;11(10):e1005253 [PMID: 26506431]
Virus Res. 2019 Jun;266:25-33 [PMID: 30959069]
PLoS Genet. 2010 Jan 22;6(1):e1000825 [PMID: 20107605]
Fly (Austin). 2012 Apr-Jun;6(2):80-92 [PMID: 22728672]
Nature. 2012 Nov 15;491(7424):393-8 [PMID: 23151582]
Genome Biol. 2013;14(9):R107 [PMID: 24070215]
Nat Rev Immunol. 2012 Apr 25;12(5):367-82 [PMID: 22531325]
Nat Methods. 2020 Feb;17(2):155-158 [PMID: 31819265]
Vet Rec. 2007 Jan 13;160(2):58-9 [PMID: 17220525]
Genome Res. 2007 Dec;17(12):1755-62 [PMID: 17989248]
J Mol Biol. 1997 Apr 25;268(1):78-94 [PMID: 9149143]
Annu Rev Anim Biosci. 2016;4:61-85 [PMID: 26526544]
Pathogens. 2021 Nov 18;10(11): [PMID: 34832656]
Science. 1990 Jun 22;248(4962):1517-23 [PMID: 2360047]
Commun Biol. 2018 Nov 16;1:197 [PMID: 30456315]
Bioinformatics. 2006 Nov 1;22(21):2688-90 [PMID: 16928733]
BMC Bioinformatics. 2012 Sep 19;13:238 [PMID: 22988817]
PLoS One. 2012;7(11):e47768 [PMID: 23185243]
Virol J. 2012 Sep 11;9:192 [PMID: 22967311]
PLoS One. 2014 Nov 19;9(11):e112963 [PMID: 25409509]
J Virol. 2011 Jun;85(12):6008-14 [PMID: 21450812]
Nat Methods. 2016 Dec;13(12):1050-1054 [PMID: 27749838]
J Gen Virol. 1998 Jun;79 ( Pt 6):1439-43 [PMID: 9634086]
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8 [PMID: 17485477]
Nat Rev Immunol. 2006 Dec;6(12):883-94 [PMID: 17110956]
Nat Methods. 2013 Jun;10(6):563-9 [PMID: 23644548]
Nat Commun. 2019 Apr 30;10(1):1992 [PMID: 31040280]
Transbound Emerg Dis. 2011 Apr;58(2):128-34 [PMID: 21294855]
Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
Cell. 2008 Aug 22;134(4):587-98 [PMID: 18724932]
Genome Biol. 2007;8(11):R245 [PMID: 18021448]
Clin Genet. 2011 Feb;79(2):103-17 [PMID: 20738327]
Nature. 2011 Jul 13;475(7357):493-6 [PMID: 21753753]
Gigascience. 2020 Mar 1;9(3): [PMID: 32191811]
Nat Genet. 2017 Apr;49(4):643-650 [PMID: 28263316]
BMC Bioinformatics. 2018 May 8;19(Suppl 6):153 [PMID: 29745866]
Bioinformatics. 2004 Nov 1;20(16):2878-9 [PMID: 15145805]
Genome Res. 2010 Jan;20(1):110-21 [PMID: 19858363]
Science. 1978 Aug 4;201(4354):460-3 [PMID: 96530]
Nat Rev Genet. 2007 Nov;8(11):857-68 [PMID: 17943193]
Nucleic Acids Res. 2021 Jul 2;49(W1):W317-W325 [PMID: 34086934]
Nat Protoc. 2009;4(7):1073-81 [PMID: 19561590]
BMC Bioinformatics. 2004 May 14;5:59 [PMID: 15144565]

MeSH Term

Animals
Swine
Phylogeny
Species Specificity
Adaptation, Physiological
Africa