Allelic diversity and patterns of selection at the major histocompatibility complex class I and II loci in a threatened shorebird, the Snowy Plover (Charadrius nivosus)

Medardo Cruz-López,Guillermo Fernández,Oscar Gonzalez,Raya Pruner,Eduardo Palacios,Salvador Gómez Del Angel,Terry Burke,Helen Hipperson,Clemens Küpper,Daniel Galindo-Espinosa,John Cavitt

doi:10.1186/s12862-020-01676-7

Abstract

BackgroundUnderstanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. Typically, classical MHC genes show high polymorphism and are under strong balancing selection, as their products trigger the adaptive immune response in vertebrates. Here, we assess the allelic diversity and patterns of selection for MHC class I and class II loci in a threatened shorebird with highly flexible mating and parental care behaviour, the Snowy Plover (Charadrius nivosus) across its broad geographic range.ResultsWe determined the allelic and nucleotide diversity for MHC class I and class II genes using samples of 250 individuals from eight breeding population of Snowy Plovers. We found 40 alleles at MHC class I and six alleles at MHC class II, with individuals carrying two to seven different alleles (mean 3.70) at MHC class I and up to two alleles (mean 1.45) at MHC class II. Diversity was higher in the peptide-binding region, which suggests balancing selection. The MHC class I locus showed stronger signatures of both positive and negative selection than the MHC class II locus. Most alleles were present in more than one population. If present, private alleles generally occurred at very low frequencies in each population, except for the private alleles of MHC class I in one island population (Puerto Rico, lineage tenuirostris).ConclusionSnowy Plovers exhibited an intermediate level of diversity at the MHC, similar to that reported in other Charadriiformes. The differences found in the patterns of selection between the class I and II loci are consistent with the hypothesis that different mechanisms shape the sequence evolution of MHC class I and class II genes. The rarity of private alleles across populations is consistent with high natal and breeding dispersal and the low genetic structure previously observed at neutral genetic markers in this species.

Highlights

Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics
When we compared the nucleotide diversity at the Peptide-binding region (PBR) sites, we found that the MHC class I showed moderately higher values of diversity (0.16 ± 0.03) than at MHC class II (0.12 ± 0.03)
Consistent with this, we found that sites with signatures of purifying selection were predominantly non-PBR sites, whereas five of the six sites under diversifying selection in the MHC class I and in one site at MHC class II corresponded to PBR sites

Summary

Introduction

Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. The genes of the major histocompatibility complex (MHC) are crucial for the immune response in vertebrates [1, 2] Their encoded proteins are involved in presenting antigen derived from pathogens to immune cells, which trigger a cascade of immune responses [3, 4]. Because of their functional importance and the direct link between MHC diversity, fitness and individual behaviour [3, 5], the MHC has been the subject of ecological and evolutionary studies ranging from assessing individual survival and mate choice to the processes of speciation and practical conservation management [6,7,8,9,10]. The maintenance of MHC diversity is crucial for pathogen resistance, which represents one of the principal selective forces impacting fitness and long-term survival of endangered species [2, 12]

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