Major histocompatibility complex alleles associated with parasite susceptibility in wild giant pandas

Abstract

Major histocompatibility complex (MHC) polymorphism is thought to be driven by antagonistic coevolution between pathogens and hosts, mediated through either overdominance or frequency-dependent selection. However, investigations under natural conditions are still rare for endangered mammals which often exhibit depleted variation, and the mechanism of selection underlying the maintenance of characteristics remains a considerable debate. In this study, 87 wild giant pandas were used to investigate MHC variation associated with parasite load. With the knowledge of the MHC profile provided by the genomic data of the giant panda, seven DRB1, seven DQA1 and eight DQA2 alleles were identified at each single locus. Positive selection evidenced by a significantly higher number of non-synonymous substitutions per non-synonymous codon site relative to synonymous substitutions per synonymous codon site could only be detected at the DRB1 locus, which leads to the speculation that DRB1 may have a more important role in dealing with parasite infection for pandas. Coprological analyses revealed that 55.17% of individuals exhibited infection with 1-2 helminthes and 95.3% of infected pandas carried Baylisascaris shroederi. Using a generalized linear model, we found that Aime-DRB1*10 was significantly associated with parasite infection, but no resistant alleles could be detected. MHC heterozygosity of the pandas was found to be uncorrelated with the infection status or the infection intensity. These results suggested that the possible selection mechanisms in extant wild pandas may be frequency dependent rather than being determined by overdominance selection. Our findings could guide the candidate selection for the ongoing reintroduction or translocation of pandas.

Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

“…However, gene duplication at the DRB1 locus limits the use of this data set. Specific MHC alleles have been linked to disease susceptibility in other host-pathogen systems, including amphibian resistance to the pathogenic fungus Batrachochytridium dendrobatidis and the susceptibility of giant pandas (Ailuropoda melanoleuca) to intestinal parasitic infections (Savage and Zamudio 2011;Bataille et al 2015;Zhang et al 2015). Sequencing approaches that can distinguish between alleles from duplicated genes are required to further test the hypothesis that WNS exerts immunogenetic selection.…”

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations

“…Some MHC genes have revealed astoundingly high levels of variation in many species (Klein 1986;Hughes and Yeager 1998). Empirical data suggests that positive, parasite-driven selection underlies this high variation whereby the exact mechanism behind the positive selection is still debated (Paterson et al 2004;Sommer 2005;Piertney and Oliver 2006;Zhang et al 2015). Nonetheless, the high variability and adaptive significance of MHC genes make them ideal candidates to study selection pressure in non-model species (e.g.…”

Major histocompatibility complex classII DABalleles associated with intestinal parasite load in the vulnerable Chinese egret (Egretta eulophotes)

“…; Zhang et al. ). A positive relationship was observed between the allele Egeu ‐DAB2*05 and parasite load, and no significant associations were found in all other alleles.…”

“…; Zhang et al. ). In past, the rare‐allele advantage hypothesis has been well supported by evidence for the associations between particular alleles and susceptibility/resistance to infection, in a wide range of vertebrate taxa (e.g., Paterson et al.…”

“…; Zhang et al. ) including some bird species, including Passer domesticus (Loiseau et al. ), Geothlypis trichas (Dunn et al.…”