Major histocompatibility complex selection dynamics in pathogen-infected túngara frog ( Physalaemus pustulosus ) populations

Abstract

Pathogen-driven selection can favour major histocompatibility complex (MHC) alleles that confer immunological resistance to specific diseases. However, strong directional selection should deplete genetic variation necessary for robust immune function in the absence of balancing selection or challenges presented by other pathogens. We examined selection dynamics at one MHC class II (MHC-II) locus across Panamanian populations of the tú ngara frog, Physalaemus pustulosus, infected by the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). We compared MHC-II diversity in highland tú ngara frog populations, where amphibian communities have experienced declines owing to Bd, with those in the lowland region that have shown no evidence of decline. Highland region frogs had MHC variants that confer resistance to Bd. Variant fixation appeared to occur by directional selection rather than inbreeding, as overall genetic variation persisted in populations. In Bd-infected lowland sites, however, selective advantage may accrue to individuals with only one Bd-resistance allele, which were more frequent. Environmental conditions in lowlands should be less favourable for Bd infection, which may reduce selection for specific Bd resistance in hosts. Our results suggest that MHC selection dynamics fluctuate in tú ngara frog populations as a function of the favourability of habitat to pathogen spread and the vulnerability of hosts to infection.

Ancestral chytrid pathogen remains hypervirulent following its long coevolution with amphibian hosts

“…North American Rana yavapaiensis show similar patterns of MHC-based resistance [30,71]. Panamanian Engystomops pustulosus are more likely to show such conformations in highland habitats favourable to Bd growth and transmission, as frogs there are most at risk of infection and disease [72]. The resistance mounted by Korean species to Bd in our study thus might be attributable to their evolved innate immunity, adaptive immunity or both.…”

A cold-blooded view of adaptive immunity

“…Several studies, however, have also implicated adaptive immune mechanisms, specifically MHC polymorphisms, that correlate with susceptibility or resistance to the chytrid fungus 217,218 .…”

Blood parasites shape extreme major histocompatibility complex diversity in a migratory passerine

“…While many studies have shown that specific MHC alleles can be associated with increased or decreased parasite load (Aguilar et al, 2016;Bateson et al, 2016;Bonneaud et al, 2006;Kloch et al, 2010;Kosch et al, 2016;Meyer-Lucht & Sommer, 2005Savage & Zamudio, 2011;Sepil et al, 2013;Teacher et al, 2009;Westerdahl et al, 2012), the consequences that such associations may have for changes in MHC allele frequencies have been less well studied (but see Westerdahl et al, 2004). Perhaps the best example that we are aware of is an experimental study in sticklebacks (Gasterosteus aculeatus) showing a rapid shift of MHC allele frequencies in response to parasite-mediated selection over just one generation (Eizaguirre, Lenz, Kalbe, & Milinski, 2012b (Kloch et al, 2010;Madsen & Ujvari, 2006;Wegner, Kalbe, Milinski, & Reusch, 2008; , but are consistent with positive associations between MHC allele number and resistance to avian malaria reported for collared flycatchers Ficedula albicollis and great reed warblers Acrocephalus arundinaceus (Radwan et al, 2012;Westerdahl et al, 2005).…”

“…MHC variants (alleles, genotypes, supertypes) and infection status/ intensity (e.g., Aguilar et al, 2016;Bateson et al, 2016;Bonneaud, P erez-Tris, Federici, Chastel, & Sorci, 2006;Kloch, Babik, Bajer, Si nski, & Radwan, 2010;Kosch et al, 2016;Meyer-Lucht & Sommer, 2005Savage & Zamudio, 2011;Sepil, Lachish, Hinks, & Sheldon, 2013;Teacher, Garner, & Nichols, 2009;Westerdahl, Asghar, Hasselquist, & Bensch, 2012). Such associations suggest that pathogens exert selection pressure on MHC genotypes, which should be reflected in temporal changes in MHC allele frequencies.…”