Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

Winternitz, Jamie; Minchey, Sergio; Garamszegi, László Zsolt; Huang, Siqi; Stephens, Patrick R.; Altizer, Sonia

doi:10.1098/rspb.2013.1605

Cited by 61 publications

(74 citation statements)

References 76 publications

(117 reference statements)

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“…HLA class 1 molecules have also been shown to have a role in both neurodevelopment (29) and mate selection (30). It is thus possible that HLA-B27 has a selective developmental or reproductive advantage that maintains its prevalence in multiple human populations despite the almost certain evolutionary disadvantages associated with increased SpA prevalence.…”

Section: Other Functions Of Hla-b27 Heterotrimers and Free Heavy Chainsmentioning

confidence: 99%

Hla-B27

Bowness

2015

Annu. Rev. Immunol.

227

169

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Possession of the human leukocyte antigen (HLA) class I molecule B27 is strongly associated with ankylosing spondylitis (AS), but the pathogenic role of HLA-B27 is unknown. Two broad theories most likely explain the role of HLA-B27 in AS pathogenesis. The first is based on the natural immunological function of HLA-B27 of presenting antigenic peptides to cytotoxic T cells. Thus, HLA-B27-restricted immune responses to self-antigens, or arthritogenic peptides, might drive immunopathology. B27 can also "behave badly," misfolding during assembly and leading to endoplasmic reticulum stress and autophagy responses. β2m-free B27 heavy chain structures including homodimers (B272) can also be expressed at the cell surface following endosomal recycling of cell surface heterotrimers. Cell surface free heavy chains and B272 bind to innate immune receptors on T, NK, and myeloid cells with proinflammatory effects. This review describes the natural function of HLA-B27, its disease associations, and the current theories as to its pathogenic role.

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Section: Other Functions Of Hla-b27 Heterotrimers and Free Heavy Chainsmentioning

confidence: 99%

Hla-B27

Bowness

2015

Annu. Rev. Immunol.

227

169

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“…A recent comparative and meta‐analysis even suggests that sexual selection may contribute more to the maintenance of MHC variation than pathogens (Winternitz et al . ). The association of MHC genes with sexual selection is typically explained through a couple of ultimate mechanisms.…”

Section: Introductionmentioning

confidence: 97%

A quantitative review of MHC‐based mating preference: the role of diversity and dissimilarity

et al. 2014

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Sexual selection hypotheses stipulate that the major histocompatibility complex genes (MHC) constitute a key molecular underpinning for mate choice in vertebrates. The last four decades saw growing empirical literature on the role of MHC diversity and dissimilarity in mate choice for a wide range of vertebrate animals, but with mixed support for its significance in natural populations. Using formal phylogenetic metaanalysis and meta-regression techniques, we quantitatively review the existing literature on MHC-dependent mating preferences in nonhuman vertebrates with a focus on the role of MHC diversity and dissimilarity. Overall, we found small, statistically nonsignificant, average effect sizes for both diversity-and dissimilarity-based mate choice (r = 0.113 and 0.064, respectively). Importantly, however, meta-regression models revealed statistically significant support regarding female choice for diversity, and choice for dissimilarity (regardless of choosy sex) only when dissimilarity is characterized across multiple loci. Little difference was found among vertebrate taxa; however, the lack of statistical power meant statistically significant effects were limited to some taxa. We found little sign of publication bias; thus, our results are likely to be robust. In light of our quantitative assessment, methodological improvements and fruitful future avenues of research are highlighted.

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“…MHC molecules are membrane receptors that, according to the current paradigm, present peptides of intracellular (MHC class I) or extracellular (MHC class II) origin to immune-surveillance-dedicated cells such as T lymphocytes6. As a consequence, an individual’s ability to recognize and resist a broad spectrum of potential pathogens tends to correlate with the diversity of its MHC alleles89 (but see the study by Milinski10). In this context, the evolutionary benefits of MHC-dependent mate choice are straightforward: choosy individuals preferring MHC-dissimilar mates are expected to produce offspring with higher fitness.…”

mentioning

confidence: 99%

“…In fact, various studies found that MHC-dependent mate choice had a positive effect on parasite load and survival rates of juveniles1112 and also ultimately on offspring fitness13. Except for some recently published cases of MHC-assortative choice1415, MHC-disassortative mate choice has been found in many vertebrate species, including fish1116, reptiles17, birds18 and mammals4919.…”

mentioning

confidence: 99%

MHC-dependent mate choice is linked to a trace-amine-associated receptor gene in a mammal

Santos

Courtiol

Heidel

et al. 2016

Sci Rep

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Major histocompatibility complex (MHC) genes play a pivotal role in vertebrate self/nonself recognition, parasite resistance and life history decisions. In evolutionary terms, the MHC’s exceptional diversity is likely maintained by sexual and pathogen-driven selection. Even though MHC-dependent mating preferences have been confirmed for many species, the sensory and genetic mechanisms underlying mate recognition remain cryptic. Since olfaction is crucial for social communication in vertebrates, variation in chemosensory receptor genes could explain MHC-dependent mating patterns. Here, we investigated whether female mate choice is based on MHC alleles and linked to variation in chemosensory trace amine-associated receptors (TAARs) in the greater sac-winged bat (Saccopteryx bilineata). We sequenced several MHC and TAAR genes and related their variation to mating and paternity data. We found strong evidence for MHC class I-dependent female choice for genetically diverse and dissimilar males. We also detected a significant interaction between mate choice and the female TAAR3 genotype, with TAAR3-heterozygous females being more likely to choose MHC-diverse males. These results suggest that TAARs and olfactory cues may be key mediators in mammalian MHC-dependent mate choice. Our study may help identify the ligands involved in the chemical communication between potential mates.

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Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

Cited by 61 publications

References 76 publications

Hla-B27

Hla-B27

A quantitative review of MHC‐based mating preference: the role of diversity and dissimilarity

MHC-dependent mate choice is linked to a trace-amine-associated receptor gene in a mammal

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