Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana).

Mao-Fang Luo,Hui-Juan Pan,Zhi-Jin Liu,Ming Li

doi:10.1186/1471-2148-12-207

Abstract

BackgroundSmall, isolated populations often experience loss of genetic variation due to random genetic drift. Unlike neutral or nearly neutral markers (such as mitochondrial genes or microsatellites), major histocompatibility complex (MHC) genes in these populations may retain high levels of polymorphism due to balancing selection. The relative roles of balancing selection and genetic drift in either small isolated or bottlenecked populations remain controversial. In this study, we examined the mechanisms maintaining polymorphisms of MHC genes in small isolated populations of the endangered golden snub-nosed monkey (Rhinopithecus roxellana) by comparing genetic variation found in MHC and microsatellite loci. There are few studies of this kind conducted on highly endangered primate species.ResultsTwo MHC genes were sequenced and sixteen microsatellite loci were genotyped from samples representing three isolated populations. We isolated nine DQA1 alleles and sixteen DQB1 alleles and validated expression of the alleles. Lowest genetic variation for both MHC and microsatellites was found in the Shennongjia (SNJ) population. Historical balancing selection was revealed at both the DQA1 and DQB1 loci, as revealed by excess non-synonymous substitutions at antigen binding sites (ABS) and maximum-likelihood-based random-site models. Patterns of microsatellite variation revealed population structure. FST outlier analysis showed that population differentiation at the two MHC loci was similar to the microsatellite loci.ConclusionsMHC genes and microsatellite loci showed the same allelic richness pattern with the lowest genetic variation occurring in SNJ, suggesting that genetic drift played a prominent role in these isolated populations. As MHC genes are subject to selective pressures, the maintenance of genetic variation is of particular interest in small, long-isolated populations. The results of this study may contribute to captive breeding and translocation programs for endangered species.

Highlights

Small, isolated populations often experience loss of genetic variation due to random genetic drift
Understanding how levels of genetic variation influence the survival of threatened species is of fundamental interest to evolutionary and conservation biologists because many natural populations are threatened by intense reduction and fragmentation of habitat, leading to isolation, declining populations, and decreasing genetic diversity [1,2]
Other research has found low levels of detectable polymorphisms for major histocompatibility complex (MHC) genes in populations with lower diversity in neutral markers, including studies on fallow deer (Cervus dama) [18], northern elephant seals (Mirounga angustirostris) [19], great crested newt (Triturus cristatus) [20], and the blackfooted rock-wallaby (Petrogale lateralis lateralis) [21]. These results suggest that compared to genetic drift balancing selection is relatively weak in small populations, leading to reduced variation at some MHC loci [22]

Summary

Introduction

Small, isolated populations often experience loss of genetic variation due to random genetic drift. We examined the mechanisms maintaining polymorphisms of MHC genes in small isolated populations of the endangered golden snub-nosed monkey (Rhinopithecus roxellana) by comparing genetic variation found in MHC and microsatellite loci. Understanding how levels of genetic variation influence the survival of threatened species is of fundamental interest to evolutionary and conservation biologists because many natural populations are threatened by intense reduction and fragmentation of habitat, leading to isolation, declining populations, and decreasing genetic diversity [1,2]. The small population size and fixation of deleterious alleles leads to inbreeding depression and reduction of individual fitness, which decreases viability and compromises a population’s evolutionary adaptive potential [6]

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Conclusion