Balancing selection, genetic drift, and human-mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout.

Lorenzo Talarico,Anna Rita Rossi,Gerardo Petrosino,Lorenzo Tancioni,Silvio Marta,Simone Crescenzo,Marco Martinoli

doi:10.1002/ece3.7760

Abstract

The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen‐mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC‐DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human‐mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance.

Highlights

The major histocompatibility complex (MHC) is an extraordinarily polymorphic, gene-rich family involved in the immune response of vertebrates
Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human-mediated introgression in shaping the pattern of MHC variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance
The relationship between multiple components of MHC diversity and body condition was tested through mixed-effect models (Table 4), which showed that (a) the within-population frequency of MHC alleles and supertypes carried by an individual was negatively associated with its body condition, while zygosity was unrelated with body condition for either MHC-DAB and MHC-ST; and (b) nucleotide and amino acid dissimilarity between MHC sequences carried by an individual was not a significant predictor of body condition

Summary

Introduction

The major histocompatibility complex (MHC) is an extraordinarily polymorphic, gene-rich family involved in the immune response of vertebrates. Proteins encoded by classical MHC genes recognize and bind antigens derived from parasites and pathogens initiating the adaptive immune cascade (Kaufman, 2018). The range of antigens that a MHC protein can recognize is determined by the amino acid composition of particular highly variable sites, referred to as antigen- binding sites, encoded by the exon 2 in classical MHC class II genes. Given the adaptive significance and the long-time persistence of MHC polymorphism, MHC has become a paradigm for investigating pathogen-mediated balancing selection. Two mutually non-exclusive forms of balancing selection are commonly postulated: the rare allele advantage (RAA) and the heterozygote advantage (HA) (Radwan et al, 2020; Spurgin & Richardson, 2010)

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