Biological Invasions

, Volume 19, Issue 4, pp 1255–1271 | Cite as

High adaptive variability and virus-driven selection on major histocompatibility complex (MHC) genes in invasive wild rabbits in Australia

  • Nina Schwensow
  • Camila J. Mazzoni
  • Elena Marmesat
  • Joerns Fickel
  • David Peacock
  • John Kovaliski
  • Ron Sinclair
  • Phillip Cassey
  • Brian Cooke
  • Simone Sommer
Original Paper


The rabbit haemorrhagic disease virus (RHDV) was imported into Australia in 1995 as a biocontrol agent to manage one of the most successful and devastating invasive species, the European rabbit (Oryctolagus cuniculus cuniculus). During the first disease outbreaks, RHDV caused mortality rates of up to 97% and reduced Australian rabbit numbers to very low levels. However, recently increased genetic resistance to RHDV and strong population growth has been reported. Major histocompatibility complex (MHC) class I immune genes are important for immune responses against viruses, and a high MHC variability is thought to be crucial in adaptive processes under pathogen-driven selection. We asked whether strong population bottlenecks and presumed genetic drift would have led to low MHC variability in wild Australian rabbits, and if the retained MHC variability was enough to explain the increased resistance against RHD. Despite the past bottlenecks we found a relatively high number of MHC class I sequences distributed over 2–4 loci. We identified positive selection on putative antigen-binding sites of the MHC. We detected evidence for RHDV-driven selection as one MHC supertype was negatively associated with RHD survival, fitting expectations of frequency-dependent selection. Gene duplication and pathogen-driven selection are possible (and likely) mechanisms that maintained the adaptive potential of MHC genes in Australian rabbits. Our findings not only contribute to a better understanding of the evolution of invasive species, they are also important in the light of planned future rabbit biocontrol in Australia.


Major histocompatibility complex (MHC) Australian rabbit invasion Rabbit haemorrhagic disease virus (RHDV) Virus-driven selection Adaptive genetic variability 



We thank the Invasive Animals CRC for accommodation during the 2010 field season. This study was made possible by the Priority Programme of the German Science Foundation (DFG) ‘Host-parasite co-evolution—rapid reciprocal adaptation and its genetic basis’ (SPP 1399, PI: So 428/7-1). We thank the South Australian Research and Development Institute for access to the Turretfield Research Station. We thank two anonymous referees for very useful comments on a previous draft of the MS. NS and PC were supported by grants and fellowships from the Australian Research Council.


This study was funded by the Priority Programme of the German Science Foundation (DFG) ‘Host-parasite co-evolution—rapid reciprocal adaptation and its genetic basis’ (SPP 1399, PI: So 428/7-1).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2016_1329_MOESM1_ESM.docx (15 kb)
Supplemental Fig. 1 Nucleotide and amino acid alignment. Sequence alignment of MHC I alleles from wild rabbits from the Turretfield population/Australia. The sequence corresponds to the amino acid positions 104-168 of the α2 domain of the human MHC I sequence. Asterisks indicate putative human ABS (Bjorkman and Parham 1990; Bjorkman et al. 1987), ‘x’ indicates the positions where evidence for positive selection on the rabbit MHC alleles was identified using the indicated statistical approaches. Dots indicate identity to the top sequence. The nucleotide sequences of MHC class I-Orcu*01a, MHC class I-Orcu*01b and MHC class I-Orcu*01c translated into the same amino acid sequence. a see Table 1 for statistics, bcodons with significance level > 0.1, ccodons with Bayes factor > 50, dcodons with posterior probability ≥ 0.9. (DOCX 14 kb)
10530_2016_1329_MOESM2_ESM.docx (17 kb)
Supplementary material 2 (DOCX 16 kb)
10530_2016_1329_MOESM3_ESM.xlsx (11 kb)
Supplementary material 3 (XLSX 11 kb)


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Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Nina Schwensow
    • 1
    • 2
    • 3
  • Camila J. Mazzoni
    • 2
    • 4
  • Elena Marmesat
    • 5
  • Joerns Fickel
    • 2
    • 6
  • David Peacock
    • 7
  • John Kovaliski
    • 7
  • Ron Sinclair
    • 1
  • Phillip Cassey
    • 1
  • Brian Cooke
    • 8
  • Simone Sommer
    • 2
    • 3
  1. 1.School of Biological SciencesUniversity of AdelaideAdelaideAustralia
  2. 2.Department of Evolutionary GeneticsLeibniz Institute for Zoo and Wildlife Research (IZW)BerlinGermany
  3. 3.Institute of Evolutionary Ecology and Conservation GenomicsUniversity of UlmUlmGermany
  4. 4.Berlin Center for Genomics in Biodiversity Research Koenigin-Luise-Str. 6-8BerlinGermany
  5. 5.Department of Integrative EcologyDoñana Biological Station (EBD-CSIC)SevilleSpain
  6. 6.Molecular Ecology and EvolutionInstitute for Biochemistry and BiologyPotsdam UniversityPotsdamGermany
  7. 7.Biosecurity SAAdelaideAustralia
  8. 8.Institute for Applied EcologyUniversity of CanberraCanberraAustralia

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