Spatial Pattern of Genetic Diversity and Selection in the MHC Class II DRB of Three Neotropical Bat Species

Overview

Journal BMC Evol Biol

Publisher Biomed Central

Specialty Biology

Date 2016 Oct 27

PMID 27782798

Citations 5

Authors

Arielle Salmier

Benoit De Thoisy

Brigitte Crouau-Roy

Vincent Lacoste

Anne Lavergne

Affiliations

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Abstract

Background: Although bats are natural reservoirs of many pathogens, few studies have been conducted on the genetic variation and detection of selection in major histocompatibility complex (MHC) genes. These genes are critical for resistance and susceptibility to diseases, and host-pathogen interactions are major determinants of their extensive polymorphism. Here we examined spatial patterns of diversity of the expressed MHC class II DRB gene of three sympatric Neotropical bats, Carollia perspicillata and Desmodus rotundus (Phyllostomidae), and Molossus molossus (Molossidae), all of which use the same environments (e.g., forests, edge habitats, urban areas). Comparison with neutral marker (mtDNA D-loop) diversity was performed at the same time.

Results: Twenty-three DRB alleles were identified in 19 C. perspicillata, 30 alleles in 35 D. rotundus and 20 alleles in 28 M. molossus. The occurrence of multiple DRB loci was found for the two Phyllostomidae species. The DRB polymorphism was high in all sampling sites and different signatures of positive selection were detected depending on the environment. The patterns of DRB diversity were similar to those of neutral markers for C. perspicillata and M. molossus. In contrast, these patterns were different for D. rotundus for which a geographical structure was highlighted. A heterozygote advantage was also identified for this species. No recombination or gene conversion event was found and phylogenetic relationships showed a trans-species mode of evolution in the Phyllostomids.

Conclusions: This study of MHC diversity demonstrated the strength of the environment and contrasting pathogen pressures in shaping DRB diversity. Differences between positively selected sites identified in bat species highlighted the potential role of gut microbiota in shaping immune responses. Furthermore, multiple geographic origins and/or population admixtures observed in C. perspicillata and M. molossus populations acted as an additional force in shaping DRB diversity. In contrast, DRB diversity of D. rotundus was shaped by environment rather than demographic history.

Citing Articles

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Li X, Liu T, Li A, Xiao Y, Sun K, Feng J Evol Appl. 2023; 16(3):688-704.

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Major histocompatibility complex variation is similar in little brown bats before and after white-nose syndrome outbreak.

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Can extreme MHC class I diversity be a feature of a wide geographic range? The example of Seba's short-tailed bat (Carollia perspicillata).

Qurkhuli T, Schwensow N, Brandel S, Tschapka M, Sommer S Immunogenetics. 2019; 71(8-9):575-587.

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References

Kupfermann H, Satta Y, Takahata N, Tichy H, Klein J . Evolution of Mhc-DRB introns: implications for the origin of primates. J Mol Evol. 1999; 48(6):663-74. DOI: 10.1007/pl00006510. View

Myers N, Mittermeier R, Mittermeier C, da Fonseca G, Kent J . Biodiversity hotspots for conservation priorities. Nature. 2000; 403(6772):853-8. DOI: 10.1038/35002501. View

Yang Z, Nielsen R, Goldman N, Pedersen A . Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 2000; 155(1):431-49. PMC: 1461088. DOI: 10.1093/genetics/155.1.431. View

Ditchkoff S, Lochmiller R, MASTERS R, Hoofer S, Van Den Bussche R . Major-histocompatibility-complex-associated variation in secondary sexual traits of white-tailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution. 2001; 55(3):616-25. DOI: 10.1554/0014-3820(2001)055[0616:mhcavi]2.0.co;2. View

Katoh K, Misawa K, Kuma K, Miyata T . MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

Kennedy L, Ryvar R, Gaskell R, Addie D, Willoughby K, Carter S . Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics. 2002; 54(5):348-52. DOI: 10.1007/s00251-002-0465-5. View

Hedrick P . Pathogen resistance and genetic variation at MHC loci. Evolution. 2002; 56(10):1902-8. DOI: 10.1111/j.0014-3820.2002.tb00116.x. View

Ronquist F, Huelsenbeck J . MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19(12):1572-4. DOI: 10.1093/bioinformatics/btg180. View

Guindon S, Gascuel O . A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003; 52(5):696-704. DOI: 10.1080/10635150390235520. View

10.

Bowen L, Aldridge B, Gulland F, Van Bonn W, DeLong R, Melin S . Class II multiformity generated by variable MHC- DRB region configurations in the California sea lion ( Zalophus californianus). Immunogenetics. 2004; 56(1):12-27. DOI: 10.1007/s00251-004-0655-4. View

11.

Kosakovsky Pond S, Frost S, Muse S . HyPhy: hypothesis testing using phylogenies. Bioinformatics. 2004; 21(5):676-9. DOI: 10.1093/bioinformatics/bti079. View

12.

Yang Z, Wong W, Nielsen R . Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol. 2005; 22(4):1107-18. DOI: 10.1093/molbev/msi097. View

13.

Kosakovsky Pond S, Frost S . Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 2005; 22(5):1208-22. DOI: 10.1093/molbev/msi105. View

14.

Jensen J, Bohonak A, Kelley S . Isolation by distance, web service. BMC Genet. 2005; 6:13. PMC: 1079815. DOI: 10.1186/1471-2156-6-13. View

15.

Prugnolle F, Manica A, Charpentier M, Guegan J, Guernier V, Balloux F . Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol. 2005; 15(11):1022-7. DOI: 10.1016/j.cub.2005.04.050. View

16.

Piertney S, Oliver M . The evolutionary ecology of the major histocompatibility complex. Heredity (Edinb). 2005; 96(1):7-21. DOI: 10.1038/sj.hdy.6800724. View

17.

Sommer S . The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool. 2005; 2:16. PMC: 1282567. DOI: 10.1186/1742-9994-2-16. View

18.

Kosakovsky Pond S, Posada D, Gravenor M, Woelk C, Frost S . Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 2006; 23(10):1891-901. DOI: 10.1093/molbev/msl051. View

19.

Schaschl H, Wandeler P, Suchentrunk F, Obexer-Ruff G, Goodman S . Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity (Edinb). 2006; 97(6):427-37. DOI: 10.1038/sj.hdy.6800892. View

20.

Van Oosterhout C, Joyce D, Cummings S, Blais J, Barson N, Ramnarine I . Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution. 2007; 60(12):2562-74. View