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Diversification of porcine MHC class II genes: evidence for selective advantage

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Abstract

The major histocompatibility complex (MHC) is an immunological gene-dense region of high diversity in mammalian species. Sus scrofa was domesticated by at least six independent events over Eurasia during the Holocene period. It has been hypothesized that the level and distribution of MHC variation in pig populations reflect genetic selection and environmental influences. In an effort to define the complexity of MHC polymorphisms and the role of selection in the generation of class II gene diversity (DQB, DRB1, and pseudogene ΨDRB3), DNA from globally distributed unrelated domestic pigs of European and Asian origins and a Suidae out-group was analyzed. The number of pseudogene alleles identified (ΨDRB3 33) was greater than those found in the expressed genes (DQB 20 and DRB1 23) but the level of observed heterozygosity (ΨDRB3 0.452, DQB 0.732, and DRB1 0.767) and sequence diversity (ΨDRB3 0.029, DQB 0.062, and DRB1 0.074) were significantly lower in the pseudogene, respectively. The substitution ratios reflected an excess of d N (DQB 1.476, DRB1 1.724, and ΨDRB3 0.508) and the persistence of expressed gene alleles suggesting the influence of balancing selection, while the pseudogene was undergoing purifying selection. The lack of a clear MHC phylogeographic tree, coupled with close genetic distances observed between the European and Asian populations (DQB 0.047 and DRB1 0.063) suggested that unlike observations using mtDNA, the MHC diversity lacks phylogeographic structure and appears to be globally uniform. Taken together, these results suggest that, despite regional differences in selective breeding and environments, no skewing of MHC diversity has occurred.

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Acknowledgments

We would like to thank the Swine Genetics International, Lieske Genetics, Birchwood Genetics Inc., United Hog Systems Inc., High Point Swine Genetics Inc., Infigen, Taiwan Livestock Research Institute, Beijing Agriculture University, United Swine Genetics, and the Omaha Zoo for providing samples. We would also like to thank Drs. D.M. Smith and C-S Ho for their critical comments and input. This work was supported in part by USDA/NRI-CSREES grant AG2001-35205-11698, USDA-ARS, and AG58-5438-2-313. E.L. was supported by the Initiative for Future Agriculture and Food Systems Grant no. 2001-52100-11527 from the USDA Cooperative State Research, Education, and Extension Service.

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Authors and Affiliations

  1. Department of Animal Sciences, University of Illinois, Urbana, IL, 61801, USA

    Erin S. Luetkemeier, Jonathan E. Beever & Lawrence B. Schook

  2. Department of Anthropology, University of Illinois, Urbana, IL, 61801, USA

    Ripan S. Malhi

  3. Institute for Genomic Biology, University of Illinois, Urbana, IL, 61801, USA

    Ripan S. Malhi & Lawrence B. Schook

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  1. Erin S. Luetkemeier
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  2. Ripan S. Malhi
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Correspondence to Lawrence B. Schook.

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Supplementary Table 1

Allelic frequency of ΨDRB3 alleles (DOC 57.0 KB)

Supplementary Figure 1

Neighbor-joining phylogeny of mitochondrial D-loop region. The evolutionary history was inferred using the neighbor-joining method with Kimura two-parameter rooted at the out-group. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. Numbers indicate bootstrap percentages (1,000 iterations). Phylogenetic analyses were conducted in MEGA4 (DOC 8.49 KB)

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Luetkemeier, E.S., Malhi, R.S., Beever, J.E. et al. Diversification of porcine MHC class II genes: evidence for selective advantage. Immunogenetics 61, 119–129 (2009). https://doi.org/10.1007/s00251-008-0348-5

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