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Independent evolution of functional MHC class II DRB genes in New World bat species

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Abstract

Genes of the major histocompatibility complex (MHC) play a pivotal role in the vertebrate immune system and are attractive markers for functional, fitness-related, genetic variation. Although bats (Chiroptera) represent the second largest mammalian order and are prone to various emerging infectious diseases, little is known about MHC evolution in bats. In the present study, we examined expressed MHC class II DRB sequences (exons 1 to 4) of New World bat species, Saccopteryx bilineata, Carollia perspicillata, Noctilio albiventris and Noctilio leporinus (only exon 2). We found a wide range of copy number variation of DRB loci with one locus detected in the genus Noctilio and up to ten functional loci observed in S. bilineata. Sequence variation between alleles of the same taxa was high with evidence for positive selection. We found statistical support for recombination or gene conversion events among sequences within the same but not between bat species. Phylogenetic relationships among DRB alleles provided strong evidence for independent evolution of the functional MHC class II DRB genes in the three investigated species, either by recent gene duplication, or homogenization of duplicated loci by frequent gene conversion events. Phylogenetic analysis of all available chiropteran DRB exon 2 sequences confirmed their monophyletic origin within families, but revealed a possible trans-species mode of evolution pattern in congeneric bat species, e.g. within the genera Noctilio and Myotis. This is the first study investigating phylogenetic relationships of MHC genes within bats and therefore contributes to a better understanding of MHC evolution in one of the most dominant mammalian order.

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Acknowledgments

We would like to thank PD Dr. Karl-Heinz Esser of the Tierärztliche Hochschule Hannover, Germany for providing a specimen of C. perspicillata for our cDNA analyses. We thank Anke Schmidt for technical laboratory assistance and Aines Castro-Prieto and Pablo Santos for helpful comments on earlier versions of the manuscript. We further thank Charles Gunn for linguistic advice as well as an anonymous reviewer for the constructive scientific comments on the former version of the manuscript. All capture and handling of animals as well as collection and export of samples was done in concordance with national laws. Field work and animal handling was carried out according to the protocol approved by the Smithsonian Tropical Research Institute—Institutional Animal Care and Use Committee (STRI-IUCAC). Permits were issued from the Panamanian authority Autoridad National del Ambiente (ANAM, SE/A 98-08, SEX/A78-08, SEX/A-138-08) and from the Ministerio del Ambiente y Energia, Costa Rica (MINAE, Permit Number: No 183-2008-SINAC). This work was supported by the Leibniz Institute for Zoo and Wildlife Research (IZW), Germany.

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  1. Evolutionary Genetics, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315, Berlin, Germany

    Julia Schad & Simone Sommer

  2. Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315, Berlin, Germany

    Christian C. Voigt, Sabine Greiner & Dina K. N. Dechmann

  3. Max Planck Institute of Ornithology, Vogelwarte Radolfzell, Schlossallee 2, 78315, Radolfzell, Germany

    Dina K. N. Dechmann

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  1. Julia Schad
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Schad, J., Voigt, C.C., Greiner, S. et al. Independent evolution of functional MHC class II DRB genes in New World bat species. Immunogenetics 64, 535–547 (2012). https://doi.org/10.1007/s00251-012-0609-1

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