Diversity of major histocompatibility complex of II B gene and mate choice in a monogamous and long-lived seabird, the Little Auk (Alle alle)

Abstract

The major histocompatibility complex (MHC) plays a key role in the adaptive immune system of vertebrates, and is known to influence mate choice in many species. In birds, the MHC has been extensively examined but mainly in galliforms and passerines while other taxa that represent specific ecological and evolutionary life-histories, like seabirds, are underexamined. Here, we characterized diversity of MHC Class II B exon 2 in a colonial pelagic seabird, the Little Auk (or Dovekie Alle alle). We further examined whether MHC variation could be maintained through balancing selection and disassortative mating. We found high polymorphism at the genotyped MHC fragment, characterizing 99 distinct alleles across 140 individuals from three populations. The alleles frequencies exhibited a similar skewed distribution in both sexes, with the four most commonly occurring alleles representing approximately 35% of allelic variation. The results of a Bayesian site-by-site selection analysis suggest evidence of balancing selection and no direct evidence for MHC-dependent disassortative mating preferences in the Little Auk. The latter result might be attributed to the high overall polymorphism of the examined fragment, which itself may be maintained by the large population size of the species.

Fig 1. The relative frequency (bars) of five the most frequent alleles (overall observed in >10 individuals) across the three sampling locations representing three little auk breeding colonies.

The map has been prepared in ggOceanMaps [101] and scatterpie [102] in packages R software 3.6.3 (R Core Team 2020). Map source: Natural Earth (public domain): http://www.naturalearthdata.com/.

Fig 2. Distribution of allele frequencies at genotyped MHC IIB loci in the little auk in respect to sex (Spitsbergen colony only).

Only alleles found at frequencies > 2%, in either sex, are depicted.

Fig 3. Bayesian analysis of site-by-site positive selection across an alignment of exon 2 sequences from two MHC class II B gene duplicates in the little auk.

Codons displaying decisive evidence of positive selection (Bayes factors >100) are indicated by crosses. Sites showing decisive evidence of negative selection are indicated by asterisks.

Fig 4

A-D. Results of randomization tests testing for MHC-based non-random mating. No significant effects of MHC genotype were found when assessing differences in heterozygosity (4A) or dissimilarities in amino acid composition (4C–4D). Little Auks exhibited a significant assortative mating effect based on shared alleles (4B), which may be attributed to the frequency of the most commonly genotyped allele in the population and the inability to discriminate between locus-specific alleles. Dashed vertical lines denote 95% of random distribution, whereas the solid vertical lines indicate the observed mean value. An observed value located within the 95% random distribution indicates a random mating pattern, whereas an observed mean located outside the 95% range on the right side indicates assortative mating.