Non-neutral evolution of the major histocompatibility complex class II gene DRB1 in the sac-winged bat Saccopteryx bilineata

Abstract

The immune genes of the major histocompatibility complex (MHC) are classical examples for high levels of genetic diversity and non-neutral evolution. This is particularly true for the regions containing the antigen-binding sites as, for instance, in the exon 2 of the MHC class II gene DRB. We surveyed, for the first time in the order Chiroptera, the genetic diversity within this exon in the sac-winged bat Saccopteryx bilineata. We detected 11 alleles among 85 bats, of which 79 were sampled in one population. Pairwise comparisons revealed that interallelic sequence differences ranged between 3 and 22%, although nucleotide substitutions were not evenly distributed along the exon sequence. This was most probably the result of intragenic recombination. High levels of sequence divergence and significantly more nonsynonymous than synonymous substitutions (d N /d S 41) suggest long-term balancing selection. Thus, the data are consistent with the hypothesis that recombination gives rise to new alleles at the DRB locus of the sac-winged bat, and these are maintained in the population through balancing selection. In this respect, the sac-winged bat closely resembles other mammalian species.

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.…”

“…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]. …”

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).…”

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

“…To date, not much is known about the genetic structure and polymorphism of the MHC in bats (Meyer and Brunner, 2007) mainly because of a lack of sequence data for primer design. This is astonishing given the size of the order, the importance of olfactory signals for social communication in bats and their zoonotic relevance as reservoir hosts for many pathogens.…”

“…This allelic variability is within the range of MHC class II DRB polymorphism of other mammalian species (for example, Sommer, 2005). The only other DRB gene studied in a bat, Saccopteryx bilineata, revealed a rather low allelic variability (11 alleles in 85 individuals; Meyer and Brunner, 2007). However, this might be an underestimate of the actual variability because preliminary studies on RNA and DNA with species-specific developed primers revealed evidence for at least five DRB loci in Saccopteryx bilineata (Schad et al, unpublished data).…”