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

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.

Spatial patterns of immunogenetic and neutral variation underscore the conservation value of small, isolated American badger populations

“…These results agree with a large number of studies that show balancing selection on MHC PBR sites (e.g. Biedrzycka & Radwan, ; Luo et al., ). However, maximum‐likelihood methods detect historical periods of balancing selection during the evolutionary trajectory of a species (Garrigan & Hedrick, ).…”

“…Similar empirical studies in mammalian endangered species have reported low MHC diversity in cheetahs ( Acinonyx jubatus , Castro‐Prieto et al., ), Tasmania devil ( Sarcophilus harrisii , Morris, Austin, & Belov, ), European bison ( Bison bonasus , Radwan, Kawałko, Wójcik, & Babik, ), giant panda ( Ailuropoda melanoleuca , Zhang, Wu, Hu, Wu, & Wei, ), mountain goat ( Oreamnos americanus , Shafer, Fan, Côté, & Coltman, ), and the golden snub‐nosed monkey ( Phinopithecus roxellana , Luo et al., ), but there are notable exceptions. For instance, balancing selection instead of genetic drift explained high MHC polymorphism in bottlenecked populations of the Finnish wolf ( Canis lupus , Niskanen et al., ) and in the Island fox ( Urocyon littoralis , Aguilar et al., ).…”

Genetic wealth, population health: Major histocompatibility complex variation in captive and wild ring‐tailed lemurs (Lemur catta)

“…Genetic drift may, in fact, have a stronger effect on immune system or functional genes than on neutral genetic diversity (Bateson, Whittingham, Johnson, & Dunn, ; Froeschke & Sommer, ; Marsden et al., ) or may overwhelm the influence of selection in small populations (Luo, Pan, Liu, & Li, ; Miller & Lambert, ). In some cases, MHC diversity even declines faster than does neutral diversity (Bateson et al., ; Bollmer et al., ; Ejsmond & Radwan, ; Eimes et al., ; Sutton et al., , ); however, we saw a more rapid decline of neutral diversity compared to MHC diversity in the captive ring‐tailed lemur population at the DLC.…”

Identifying refugia and corridors under climate change conditions for the Sichuan snub‐nosed monkey (Rhinopithecus roxellana) in Hubei Province, China

“…The relatively lower genetic diversity, genetically distinct status and small population size of this population makes it more vulnerable to environmental change than the other two populations Luo, Pan, Liu, & Li, 2012;Pan et al, 2009). This arboreal species lives in temperate broadleaf and coniferous forests , and the impact of climate change on vegetation is expected to decrease the availability of its suitable habitat (Luo et al, 2015;Xiang et al, 2011).…”

“…This population is considered as a stand‐alone management unit (Chang, Luo, et al, ), determined to be a group of conspecific individuals among which the degree of connectivity is sufficiently low and thus should be monitored and managed separately (Palsbøll, Bérubé, & Allendorf, ; Taylor & Dizon, ). The relatively lower genetic diversity, genetically distinct status and small population size of this population makes it more vulnerable to environmental change than the other two populations (Li et al, ; Luo, Pan, Liu, & Li, ; Pan et al, ). This arboreal species lives in temperate broadleaf and coniferous forests (Chang, Liu, Yang, Li, & Vigilant, ), and the impact of climate change on vegetation is expected to decrease the availability of its suitable habitat (Luo et al, ; Xiang et al, ).…”