Divergent allele advantage at MHC-DRB through direct and maternal genotypic effects and its consequences for allele pool composition and mating

Lenz, Tobias L.; Mueller, Birte; Trillmich, Fritz; Wolf, Jochen B. W.

doi:10.1098/rspb.2013.0714

Cited by 53 publications

(71 citation statements)

References 46 publications

(85 reference statements)

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“…; Lenz et al. ). Here, we followed this development, using the average sequence divergence between parental MHC IIB haplotypes as an estimator for individual MHC diversity of the resulting offspring, and thus were able to detect patterns of selection that may have remained elusive without these technological advancements.…”

Section: Discussionmentioning

confidence: 60%

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

et al. 2018

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Females choose specific mates in order to produce fitter offspring. However, several factors interfere with females' control over fertilization of their eggs, including sneaker males and phenotypically unpredictable allele segregation during meiosis. Mate choice at the individual level thus provides only a poor approximation for obtaining the best genetic match. Consequently, postcopulatory sperm selection by female oocytes has been proposed as a mechanism to achieve complementary combinations of parental haplotypes. Here, using controlled in vitro fertilization of three‐spined stickleback eggs, we find haplotype‐specific fertilization bias toward gametes with complementary major histocompatibility complex (MHC) immunogenes. The resulting zygote (and thus offspring) genotypes exhibit an intermediate level of individual MHC diversity that was previously shown to confer highest pathogen resistance. Our finding of haplotype‐specific gamete selection thus represents an intriguing mechanism for fine‐tuned optimization of the offspring's immune gene composition and an evolutionary advantage in the Red Queen dynamics of host‐parasite coevolution.

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Section: Discussionmentioning

confidence: 60%

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

et al. 2018

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“…This hypothesis was empirically supported several times (Richardson & Westerdahl ; Lenz et al . ). However, in our case we can only speculate whether the effect of divergent allele advantage in the continental population was stronger due to PMBS or other evolutionary mechanism.…”

Section: Discussionmentioning

confidence: 97%

Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

et al. 2016

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The extracellular subunit of the major histocompatibility complex MHCIIβ plays an important role in the recognition of pathogens and the initiation of the adaptive immune response of vertebrates. It is widely accepted that pathogen-mediated selection in combination with neutral micro-evolutionary forces (e.g. genetic drift) shape the diversity of MHCIIβ, but it has proved difficult to determine the relative effects of these forces. We evaluated the effect of genetic drift and balancing selection on MHCIIβ diversity in 12 small populations of Galápagos mockingbirds belonging to four different species, and one larger population of the Northern mockingbird from the continental USA. After genotyping MHCIIβ loci by high-throughput sequencing, we applied a correlational approach to explore the relationships between MHCIIβ diversity and population size by proxy of island size. As expected when drift predominates, we found a positive effect of population size on the number of MHCIIβ alleles present in a population. However, the number of MHCIIβ alleles per individual and number of supertypes were not correlated with population size. This discrepancy points to an interesting feature of MHCIIβ diversity dynamics: some levels of diversity might be shaped by genetic drift while others are independent and possibly maintained by balancing selection.

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“…), there is little discussion of how the relationships among the alleles of those duplicated genes might determine whether disassortative mating is needed for producing offspring whose genotypes consist of functionally divergent alleles (Lenz et al . ). This lack of theoretical development might be because most empirical studies of MHC‐disassortative mate choice use laboratory methods that assay multiple MHC loci simultaneously and thus cannot assign alleles to a particular locus (see Appendix S1, Supporting information).…”

Section: Introductionmentioning

confidence: 97%

Gene duplication and divergence produce divergent MHC genotypes without disassortative mating

et al. 2016

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Genes of the major histocompatibility complex (MHC) exhibit heterozygote advantage in immune defense, which in turn can select for MHC-disassortative mate choice. However, many species lack this expected pattern of MHC-disassortative mating. A possible explanation lies in evolutionary processes following gene duplication: if two duplicated MHC genes become functionally diverged from each other, offspring will inherit diverse multilocus genotypes even under random mating. We used locus-specific primers for high throughput sequencing of two expressed MHC Class II B genes in Leach's storm-petrels, Oceanodroma leucorhoa, and found that exon 2 alleles fall into two gene-specific monophyletic clades. We tested for disassortative versus random mating at these two functionally diverged Class II B genes, using multiple metrics and different subsets of exon 2 sequence data. With good statistical power, we consistently found random assortment of mates at MHC. Despite random mating, birds had MHC genotypes with functionally diverged alleles, averaging 13 amino acid differences in pairwise comparisons of exon 2 alleles within individuals. To test whether this high MHC diversity in individuals is driven by evolutionary divergence of the two duplicated genes, we built a phylogenetic permutation model. The model showed that genotypic diversity was strongly impacted by sequence divergence between the most common allele of each gene, with a smaller additional impact of monophyly of the two genes. Divergence of allele sequences between genes may have reduced the benefits of actively seeking MHC-dissimilar mates, in which case the evolutionary history of duplicated genes is shaping the adaptive landscape of sexual selection.

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Divergent allele advantage at MHC-DRB through direct and maternal genotypic effects and its consequences for allele pool composition and mating

Cited by 53 publications

References 46 publications

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes

Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

Gene duplication and divergence produce divergent MHC genotypes without disassortative mating

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