MHC class II DRB diversity, selection pattern and population structure in a neotropical bat species, Noctilio albiventris

Abstract

Genes of the major histocompatibility complex (MHC) have a crucial role in the immune response of vertebrates, alter the individual odour and are involved in shaping mating preferences. Pathogen-mediated selection, sexual selection and maternal-fetal interactions have been proposed as the main drivers of frequently observed high levels of polymorphism in functionally important parts of the MHC. Bats constitute the second largest mammalian order and have recently emerged as important vectors of infectious diseases. In addition, Chiroptera are interesting study subjects in evolutionary ecology in the context of olfactory communication, mate choice and associated fitness benefits. Thus, it is surprising that they belong to the least studied mammalian taxa in terms of their MHC diversity. In this study, we investigated the variability in the functionally important MHC class II gene DRB, evidence for selection and population structure in the group-living lesser bulldog bat, Noctilio albiventris, in Panama. We found a single expressed, polymorphic Noal-DRB gene. The substitution pattern of the nucleotide sequences of the 18 detected alleles provided evidence for positive selection acting above the evolutionary history of the species in shaping MHC diversity. Roosting colonies were not genetically differentiated but females showed lower levels of heterozygosity than males, which might be a sign that the sexes differ in the selection pressures acting on the MHC. This study provides the prerequisites for further investigations of the role of the individual MHC constitution in parasite resistance, olfactory communication and mate choice in N. albiventris and other bats.

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

“…( M. velifer and M. vivesi [39]), 28 from Noctilio spp. ( N. albiventris and N. leporinus [35, 37]) and 17 from S. bilineata [35, 36] . The phylogenetic tree showed six major clades (Fig.…”

“…To amplify the M. molossus DRB gene, primers designed by Richman et al [39] were modified. Primers located in conserved parts of exon 1 (JSex1.5, [37]; EX1Fd, modified from [39]), exon 2 (JS2Cape, [37]), exon 3 (EX3Rd, modified from [39]) and exon 4 (L729, [50]) were used to amplify functional MHC class II DRB alleles from the cDNA of three bats from each species, C. perspicillata , D. rotundus and M. molossus . The sequences obtained were used to design specific primers complementary to conserved parts of exon 1 (BatCMHIIF (F) and BatCMHIIF.1 (F1), Table 1) and exon 4 (BatCMHIIR (R) and BatCMHIIR.1 (R1), Table 1).…”

“…Other studies, investigating the diversity of MHC DRB , showed significant differences in the polymorphism of MHC genes between species. This polymorphism was essentially influenced by (1) a pathogen-driven selection [36], (2) a social structure driven by MHC-mediated post-copulatory mechanisms [37], (3) diversifying selection and recombination events [35, 38] and (4) geographical constraints resulting in spatial variation of pathogen-mediated selection and enhanced susceptibility to environmental changes [39, 40]. …”

Genetic variation and balancing selection at MHC class II exon 2 in cultured stocks and wild populations of orange-spotted grouper (Epinephelus coioides)

“…In our study, we detected up to four different sequences in a single individual, suggesting that at least two loci of the MHC class II β gene exist at the genome level in the orange-spotted grouper. Such a high level of gene duplication has also been reported in other fish species (Xu et al, 2010), amphibians (Hauswaldt et al, 2007), birds (Westerdahl et al, 2004), and mammals (Schad et al, 2011). The presence of these multiple loci has been argued as being one important reason for the high level of polymorphism at MHC genes (Grimholt et al, 2003), although its mechanism is still far from understood.…”

“…As an example, a much higher level of excess non-synonymous over synonymous nucleotide substitutions was observed within the PBR (encoded by exon 2) compared to the non-PBR (also encoded by exon 2) in the β chain of an MHC class II molecule, and was considered evidence for "balancing selection" (Hughes and Nei, 1988). Such a selection pattern in the PBR has been extensively reported in many species (Xu et al, 2010;Schad et al, 2011).…”