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Immunogenetics

, Volume 70, Issue 6, pp 401–417 | Cite as

Inferring the evolution of the major histocompatibility complex of wild pigs and peccaries using hybridisation DNA capture-based sequencing

  • Carol Lee
  • Marco Moroldo
  • Alvaro Perdomo-Sabogal
  • Núria Mach
  • Sylvain Marthey
  • Jérôme Lecardonnel
  • Per Wahlberg
  • Amanda Y. Chong
  • Jordi Estellé
  • Simon Y. W. Ho
  • Claire Rogel-Gaillard
  • Jaime GongoraEmail author
Original Article

Abstract

The major histocompatibility complex (MHC) is a key genomic model region for understanding the evolution of gene families and the co-evolution between host and pathogen. To date, MHC studies have mostly focused on species from major vertebrate lineages. The evolution of MHC classical (Ia) and non-classical (Ib) genes in pigs has attracted interest because of their antigen presentation roles as part of the adaptive immune system. The pig family Suidae comprises over 18 extant species (mostly wild), but only the domestic pig has been extensively sequenced and annotated. To address this, we used a DNA-capture approach, with probes designed from the domestic pig genome, to generate MHC data for 11 wild species of pigs and their closest living family, Tayassuidae. The approach showed good efficiency for wild pigs (~80% reads mapped, ~87× coverage), compared to tayassuids (~12% reads mapped, ~4× coverage). We retrieved 145 MHC loci across both families. Phylogenetic analyses show that the class Ia and Ib genes underwent multiple duplications and diversifications before suids and tayassuids diverged from their common ancestor. The histocompatibility genes mostly form orthologous groups and there is genetic differentiation for most of these genes between Eurasian and sub-Saharan African wild pigs. Tests of selection showed that the peptide-binding region of class Ib genes was under positive selection. These findings contribute to better understanding of the evolutionary history of the MHC, specifically, the class I genes, and provide useful data for investigating the immune response of wild populations against pathogens.

Keywords

Major histocompatibility complex DNA sequence capture Adaptive immunity Pigs Peccaries 

Notes

Acknowledgements

We thank the Sydney School of Veterinary Science at the University of Sydney for providing research funding for sampling and financial support, allowing J. Gongora to undertake preliminary experiments in Australia and a sabbatical period to generate data for this project at INRA. We thank INRA for making funding available from The French National Research Agency (PSC-08-GENO-CapSeqAn). All samples were provided by J. Gongora, collected by himself or accessed through Dr. Stewart Lowden, Dr. Joeke Nijboer (Rotterdam Zoo) or through collaboration with institutions in Eurasia, Africa and the Americas. Many thanks to Bertrand Bed’hom for the constructive feedback on the manuscript and for the advice on the MHC locus, and the INRA @BRIDGe platform where the hybridisation capture experiments were performed.

Supplementary material

251_2017_1048_MOESM1_ESM.docx (2.8 mb)
ESM 1 (DOCX 2.76 mb)
251_2017_1048_MOESM2_ESM.zip (6.3 mb)
ESM 2 (ZIP 188 kb)
251_2017_1048_MOESM3_ESM.zip (188 kb)
ESM 3 (ZIP 6486 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Carol Lee
    • 1
  • Marco Moroldo
    • 2
  • Alvaro Perdomo-Sabogal
    • 1
    • 3
  • Núria Mach
    • 2
  • Sylvain Marthey
    • 2
  • Jérôme Lecardonnel
    • 2
  • Per Wahlberg
    • 2
  • Amanda Y. Chong
    • 1
    • 4
  • Jordi Estellé
    • 2
  • Simon Y. W. Ho
    • 5
  • Claire Rogel-Gaillard
    • 2
  • Jaime Gongora
    • 1
    Email author
  1. 1.Sydney School of Veterinary Science, Faculty of ScienceThe University of SydneySydneyAustralia
  2. 2.GABI, INRA, AgroParisTechUniversité Paris-SaclayJouy-en-JosasFrance
  3. 3.Institute of Animal Science (460i), Department of BioinformaticsUniversity of HohenheimStuttgartGermany
  4. 4.Earlham Institute, Norwich Research ParkNorwichUK
  5. 5.School of Life and Environmental Sciences, Faculty of ScienceThe University of SydneySydneyAustralia

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