Spatial pattern of genetic diversity and selection in the MHC class II DRB of three Neotropical bat species

Abstract

BackgroundAlthough 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.ResultsTwenty-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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0802-1) contains supplementary material, which is available to authorized users.

MHC class II DRB variability in wild black howler monkeys (Alouatta pigra), an endangered New World primate

“…The number of alleles detected per animal ranged from two to eight, indicating the existence of at least four DRB loci in A. pigra. This variation in the number of MHC-DRB loci between individuals of a species has been reported for several mammals, such as humans, other non-human primates, bats, tree shrews, and voles (Bontrop, 2006;Oppelt et al, 2010;Kloch et al, 2010;Salmier et al, 2016). These gene duplications contribute to MHC diversity and are known to play an important role in the adaptive evolution of organisms (Hughes and Yeager, 1998).…”

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

“…Therefore, these 4 alleles and the corresponding 5 samples were removed from analysis, leaving 131 successfully genotyped individuals with 45 nucleotide alleles and 27 amino acid alleles. We identified 1 to 5 alleles (average 2 alleles) per individual, suggesting up to 3 loci of the DRB gene in the little brown bat (Table 1) and in line with observations of 1 to 3 loci in previously studied bat species (Mayer & Brunner, 2007;Real-Monroy et al, 2014;Richman et al, 2010;Salmier et al, 2016;Schad et al, 2011Schad et al, , 2012, except for the sac-winged bat which was identified with 10 loci (Schad et al, 2012). A significant but weak correlation (R 2 = 0.11, p < .01) was detected between the sequencing depth and the number of nucleotide alleles ( Figure S1), suggesting dropout of low-depth putative alleles due to differential amplification efficiency.…”

“…Sequences translated into premature stop codons were removed from analysis, together with the samples in which these variants were found. vivesi (Richman et al, 2010), Noctilio albiventris (Schad et al, 2012), Saccopteryx bilineata (Schad et al, 2012), Carollia perspicillata (Schad et al, 2012), Desmodus rotundus (Salmier et al, 2016), and Artibeus jamaicensis (Real-Monroy et al, 2014). Codons of the antigen-binding sites were identified based on previous publications (Richman et al, 2010;Salmier et al, 2016).…”

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

“…These genes are affected by pathogen-mediated selection in a wide range of vertebrate species (Wegner et al 2003;Piertney and Oliver 2006;Savage and Zamudio 2011), and spatial patterns of variation in the MHC can serve as an immunogenetic proxy for the potential of a declining population to adapt to shifting selection by pathogens (Hawley and Fleischer 2012;Kyle et al 2014). The MHC has been studied in several bats, including a suite of Neotropical phyllostomid species (Schad et al 2012b;Real-Monroy et al 2014;Salmier et al 2016), the sac-winged bat (Saccopteryx bilineata; Mayer and Brunner 2007), and two North American Myotis species (M. velifer, M. velesi;Richman et al 2010). MHC variants are correlated with ectoparasite load in the lesser bulldog bat (Noctilio albiventris; Schad et al 2012a).…”