Spatially variable coevolution between a haemosporidian parasite and the MHC of a widely distributed passerine

Abstract

The environment shapes host–parasite interactions, but how environmental variation affects the diversity and composition of parasite-defense genes of hosts is unresolved. In vertebrates, the highly variable major histocompatibility complex (MHC) gene family plays an essential role in the adaptive immune system by recognizing pathogen infection and initiating the cellular immune response. Investigating MHC-parasite associations across heterogeneous landscapes may elucidate the role of spatially fluctuating selection in the maintenance of high levels of genetic variation at the MHC. We studied patterns of association between an avian haemosporidian blood parasite and the MHC of rufous-collared sparrows (Zonotrichia capensis) that inhabit environments with widely varying haemosporidian infection prevalence in the Peruvian Andes. MHC diversity peaked in populations with high infection prevalence, although intra-individual MHC diversity was not associated with infection status. MHC nucleotide and protein sequences associated with infection absence tended to be rare, consistent with negative frequency-dependent selection. We found an MHC variant associated with a ∽26% decrease in infection probability at middle elevations (1501–3100 m) where prevalence was highest. Several other variants were associated with a significant increase in infection probability in low haemosporidian prevalence environments, which can be interpreted as susceptibility or quantitative resistance. Our study highlights important challenges in understanding MHC evolution in natural systems, but may point to a role of negative frequency-dependent selection and fluctuating spatial selection in the evolution of Z. capensisMHC.

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

“…In testing for the maintenance hypotheses of MHC polymorphism, the Chinese egret had a negative association between MHC-specific allele and parasite load, which is similar to previous reports on other bird species, including P. domesticus (Loiseau et al 2008), G. trichas (Dunn et al 2013), C. caeruleus (Westerdahl et al 2013), and Z. capensis (Jones et al 2015). In this egret, the allele Egeu-DAB2*05 was significantly linked to uninfected individuals, and individuals carrying Egeu-DAB2*05 had significantly lower HMI values and FEC values.…”

“…), and Z. capensis (Jones et al. ). In this egret, the allele Egeu ‐DAB2*05 was significantly linked to uninfected individuals, and individuals carrying Egeu ‐DAB2*05 had significantly lower HMI values and FEC values.…”

“…This negative frequency-dependent co-evolutionary process between hosts and pathogens maintains MHC polymorphism within a population (Jeffery and Bangham 2000;Westerdahl et al 2012;Zhang et al 2015). 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 1998;Godot et al 2000;Langefors et al 2001;Schad et al 2005Schad et al , 2012Kloch et al 2010;Zhang and He 2013;Kamath et al 2014;Sin et al 2014;Zhang et al 2015) including some bird species, including Passer domesticus (Loiseau et al 2008), Geothlypis trichas (Dunn et al 2013), Cyanistes caeruleus (Westerdahl et al 2013) and Zonotrichia capensis (Jones et al 2015).…”

Major histocompatibility complex variation and blood parasites in resident and migratory populations of the common yellowthroat

“…Factors that influence the diversity and transmission of parasites, such as degree of sociality (Hambuch & Lacey, 2002;Sommer et al, 2002) or environmental conditions (Cohen, 2002;Wegner et al, 2003;Radwan et al, 2014;Jones et al, 2015), are also correlated with variation in MHC diversity. For example, MHC class II allelic diversity follows a latitudinal gradient in Atlantic salmon (Salmo salar), with greater allelic diversity associated with increasing temperature (decreasing latitude) and bacterial diversity (Dionne et al, 2007).…”

Specific MHC class I supertype associated with parasite infection and color morph in a wild lizard population

“…Evidence for parasite‐mediated selection acting on MHC genes via rare‐allele advantage (Borghans, Beltman, & De Boer, ; Schwensow et al., ), fluctuating selection (Jones, Cheviron, & Carling, ; Osborne, Pilger, Lusk, & Turner, ), heterozygote advantage (Doherty & Zinkernagel, ; Takahata & Nei, ), and optimal intermediate diversity advantage (Wegner, Kalbe, Kurtz, Reusch, & Milinski, ) has been uncovered across a range of taxa. However, most evidence points toward rare‐allele advantage and fluctuating selection as the dominant mechanisms by which pathogen‐mediated selection maintains MHC diversity, with little evidence that heterozygote advantage alone can account for the extreme diversity found at MHC loci (De Boer, Borghans, van Boven, Kesmir, & Weissing, ).…”