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. 2018 Mar 13;18(1):29.
doi: 10.1186/s12862-018-1148-7.

High polymorphism in MHC-DRB genes in golden snub-nosed monkeys reveals balancing selection in small, isolated populations

Pei Zhang  1 , Kang Huang  1 , Bingyi Zhang  1 , Derek W Dunn  1 , Dan Chen  2 , Fan Li  1 , Xiaoguang Qi  1 , Songtao Guo  1 , Baoguo Li  3   4
Affiliations

High polymorphism in MHC-DRB genes in golden snub-nosed monkeys reveals balancing selection in small, isolated populations

Pei Zhang et al. BMC Evol Biol. .

Abstract

Background: 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 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.

Results: We 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.

Conclusions: High 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.

Keywords: Balancing selection; Genetic diversity; MHC; Rhinopithecus roxellana.

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Conflict of interest statement

Ethics approval and consent to participate

All samples were collected with an ethical permission from the animal care committee of the Wildlife Protection Society of China (SL-2012-42).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Distribution of the three R. roxellana populations used for this study. The range of coordinates were 107.8°-108.5°E, 33.5°-34.0°N, UTM projection
Fig. 2
Fig. 2
Phylogenetic relationships of Rhro-DRB alleles conducted using Bayesian approach (a) and maximum likelihood method (b). Orthologous sequences from Ovis aries (Ovar-DRB1*0101), Macaca fascicularis (Mafa-DRB), Macaca mulatta (Mamu-DRB), Mandrillus sphinx (Masp-DRB), Pan troglodytes (Patr-DRB), Gorilla gorilla (Gogo-DRB) and Homo sapiens (HLA-DRB) were include in the analysis. Values on the branch are represented for the posterior probability of the Bayesian tree and the support rate of the ML tree. Sequences labeled with solid circles are DRB alleles from R. roxellana. Colored circles indicate sequences detected in the three study populations. Red ones indication Rhro-DRB1 alleles, while blue ones indicate Rhro-DRB2 alleles
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