Abstract
BackgroundMaintaining variation in immune genes, such as those of the major histocompatibility complex (MHC), is important for individuals in small, isolated populations to resist pathogens and parasites. The golden snub-nosed monkey (Rhinopithecus roxellana), an endangered primate endemic to China, has experienced a rapid reduction in numbers and severe population fragmentation over recent years. For this study, we measured the DRB diversity among 122 monkeys from three populations in the Qinling Mountains, and estimated the relative importance of different agents of selection in maintaining variation of DRB genes.ResultsWe identified a total of 19 DRB sequences, in which five alleles were novel. We found high DRB variation in R. roxellana and three branches of evidence suggesting that balancing selection has contributed to maintaining MHC polymorphism over the long term in this species: i) different patterns of both genetic diversity and population differentiation were detected at MHC and neutral markers; ii) an excess of non-synonymous substitutions compared to synonymous substitutions at antigen binding sites, and maximum-likelihood-based random-site models, showed significant positive selection; and iii) phylogenetic analyses revealed a pattern of trans-species evolution for DRB genes.ConclusionsHigh levels of DRB diversity in these R. roxellana populations may reflect strong selection pressure in this species. Patterns of genetic diversity and population differentiation, positive selection, as well as trans-species evolution, suggest that pathogen-mediated balancing selection has contributed to maintaining MHC polymorphism in R. roxellana over the long term. This study furthers our understanding of the role pathogen-mediated balancing selection has in maintaining variation in MHC genes in small and fragmented populations of free-ranging vertebrates.
Highlights
Maintaining variation in immune genes, such as those of the major histocompatibility complex (MHC), is important for individuals in small, isolated populations to resist pathogens and parasites
DRB allele assignment We examined the variation of DRB genes of 122 R. roxellana monkeys from three populations (FP, NS and ZZ)
Two to four alleles were detected in each individual, indicating at least two loci were amplified, which was consistent with previous research [30]
Summary
Maintaining variation in immune genes, such as those of the major histocompatibility complex (MHC), is important for individuals in small, isolated populations to resist pathogens and parasites. The major histocompatibility complex (MHC) gene family is one of the most polymorphic gene regions yet found in any vertebrate genome [1]. This multigene family plays a central role in the immune systems of many vertebrates by first recognizing foreign antigens and binding and presenting them to T cells, triggering an appropriate immune response [2, 3]. Pathogenmediated balancing selection is a major agent shaping MHC polymorphism as a consequence of an arms-race between pathogens and the host’s immune system [9]
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