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MHC class II β exon 2 variation in pardalotes (Pardalotidae) is shaped by selection, recombination and gene conversion

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Abstract

The high levels of polymorphism and allelic diversity which characterise genes in the major histocompatibility complex (MHC) are thought to be generated and maintained through the combined effects of different evolutionary processes. Here, we characterised exon 2 of the MHC class II β genes in two congeneric passerine species, the spotted (Pardalotus punctatus) and striated pardalote (Pardalotus striatus). We estimated the levels of allelic diversity and tested for signatures of recombination, gene conversion and balancing selection to determine if these processes have influenced MHC variation in the two species. Both species showed high levels of polymorphism and allelic diversity, as well as evidence of multiple gene loci and putative pseudogenes based on the presence of stop codons. We found higher levels of MHC diversity in the striated pardalote than the spotted pardalote, based on the levels of individual heterozygosity, sequence divergence and number of polymorphic sites. The observed differences may reflect variable selection pressure on the species, resulting from differences in patterns of movement among populations. We identified strong signatures of historical balancing selection, recombination and gene conversion at the sequence level, indicating that MHC variation in the two species has been shaped by a combination of processes.

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Acknowledgments

We thank all the members of the Birds Linkage team, especially A. Lill and N. Takeuchi, and numerous volunteers for assistance with fieldwork, as well as K. Harrisson for helpful comments on the manuscript. Samples were collected under permits from the Victorian Department of Environment and Primary Industries (numbers 10004294 under the Wildlife Act 1975 and the National Parks Act 1975, and NWF10455 under section 52 of the Forest Act 1958), the Australian Bird and Bat Banding Schemes and under approval and monitoring of Monash University ethics processes (BSCI/2007/07). This work was supported by the Australian Research Council (LP0776322), Department of Environment and Primary Industries, Museum Victoria, Parks Victoria, the North Central and Goulburn Broken Catchment Management Authorities, University of Melbourne (SB) and the Australian Academy of Sciences (JM).

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Authors and Affiliations

  1. Department of Sciences, Museum Victoria, Melbourne, Victoria, 3001, Australia

    Shandiya Balasubramaniam & Jane Melville

  2. School of BioSciences, The University of Melbourne, Melbourne, Victoria, 3010, Australia

    Shandiya Balasubramaniam & Raoul A. Mulder

  3. School of Biological Sciences, Monash University, Clayton Campus, Melbourne, Victoria, 3800, Australia

    Paul Sunnucks & Alexandra Pavlova

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  1. Shandiya Balasubramaniam
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  2. Raoul A. Mulder
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Correspondence to Shandiya Balasubramaniam.

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The sequence data supporting the results of this article are available in the Figshare digital repository and can be accessed at https://dx.doi.org/10.4225/49/57D0F3611D00A.

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Balasubramaniam, S., Mulder, R.A., Sunnucks, P. et al. MHC class II β exon 2 variation in pardalotes (Pardalotidae) is shaped by selection, recombination and gene conversion. Immunogenetics 69, 101–111 (2017). https://doi.org/10.1007/s00251-016-0953-7

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