In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individual's immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.

Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology

There is growing interest in the possibility that genetic compatibility may drive mate choice, including gamete choice, particularly from the perspective of understanding why females frequently mate with more than one male. Mate choice for compatibility differs from other forms of choice for genetic benefits (such as ‘good genes’) because individuals are expected to differ in their mate preferences, changing the evolutionary dynamics of sexual selection. Recent experiments designed to investigate genetic benefits of polyandry suggest that mate choice on the basis of genetic compatibility may be widespread. However, in most systems the mechanisms responsible for variation in compatibility are unknown. We review potential sources of variation in genetic compatibility and whether there is any evidence for mate choice driven by these factors. Selfish genetic elements appear to have the potential to drive mate compatibility mate choice, though as yet there is only one convincing example. There is abundant evidence for assortative mating between populations in hybrid zones, but very few examples where this is clearly a result of selection against mating with genetically less compatible individuals. There are also numerous cases of inbreeding avoidance, but little evidence that mate choice or differential fertilization success driven by genetic compatibility occurs between unrelated individuals. The exceptions to this are a handful of situations where both the alleles causing incompatibility and the alleles involved in mate choice are located in a chromosome region where recombination is suppressed. As yet there are only a few potential sources of genetic compatibility which have clearly been shown to drive mate choice. This may reflect limitations in the potential for the evolution of mate choice for genetic compatibility within populations, although the most promising sources of such incompatibilities have received relatively little research.

http://www.selfishgene.org/Tom/Papers/TTNW_MolEcol00.pdf

Genetic compatibility, mate choice and patterns of parentage: invited review.

One substantial benefit of sexual reproduction could be that it allows animals (including humans) to react rapidly to a continuously changing environmental selection pressure such as coevolving parasites. This counteraction would be most efficient if the females were able to provide their progeny with certain allele combinations for loci which may be crucial in the parasite-host arms race, for example the MHC (major histocompatibility complex). Here we show that the MHC influences both body odours and body odour preferences in humans, and that the women's preferences depend on their hormonal status. Female and male students were typed for their HLA-A, -B and -DR. Each male student wore a T-shirt for two consecutive nights. The next day, each female student was asked to rate the odours of six T-shirts. They scored male body odours as more pleasant when they differed from the men in their MHC than when they were more similar. This difference in odour assessment was reversed when the women rating the odours were taking oral contraceptives. Furthermore, the odours of MHC-dissimilar men remind the test women more often of their own actual or former mates than do the odours of MHC-similar men. This suggests that the MHC or linked genes influence human mate choice today.

/pdf/mhc-dependent-mate-preferences-in-humans-1og0pyy44l.pdf

MHC-dependent mate preferences in humans

Contrasting theories of visual attention emphasize selection by spatial location, visual features (such as motion or colour) or whole objects. Here we used functional magnetic resonance imaging (fMRI) to test key predictions of the object-based theory, which proposes that pre-attentive mechanisms segment the visual array into discrete objects, groups, or surfaces, which serve as targets for visual attention. Subjects viewed stimuli consisting of a face transparently superimposed on a house, with one moving and the other stationary. In different conditions, subjects attended to the face, the house or the motion. The magnetic resonance signal from each subject's fusiform face area, parahippocampal place area and area MT/MST provided a measure of the processing of faces, houses and visual motion, respectively. Although all three attributes occupied the same location, attending to one attribute of an object (such as the motion of a moving face) enhanced the neural representation not only of that attribute but also of the other attribute of the same object (for example, the face), compared with attributes of the other object (for example, the house). These results cannot be explained by models in which attention selects locations or features, and provide physiological evidence that whole objects are selected even when only one visual attribute is relevant.

fMRI evidence for objects as the units of attentional selection.

House mice prefer mates genetically dissimilar at the major histocompatibility complex (MHC). The highly polymorphic MHC genes control immunological self/nonself recognition; therefore, this mating preference may function to provide “good genes” for an individual's offspring. However, the evidence for MHC‐dependent mating preferences is controversial, and its function remains unclear. Here we provide a critical review of the studies on MHC‐dependent mating preferences in mice, sheep, and humans and the possible functions of this behavior. There are three adaptive hypotheses for MHC‐dependent mating preferences. First, MHC‐disassortative mating preferences produce MHC‐heterozygous offspring that may have enhanced immunocompetence. Although this hypothesis is not supported by tests of single parasites, MHC heterozygotes may be resistant to multiple parasites. Second, we propose that MHC‐dependent mating preferences enable hosts to provide a “moving target” against rapidly evolving parasites that e...

https://www.jstor.org/stable/10.1086/303166

The Evolution of Mating Preferences and Major Histocompatibility Complex Genes.

In house mice, and probably most mammals, major histocompatibility complex (MHC) gene products influence both immune recognition and individual odours in an allele-specific fashion. Although it is generally assumed that some form of pathogen-driven balancing selection is responsible for the unprecedented genetic diversity of MHC genes, the MHC-based mating preferences observed in house mice are sufficient to account for the genetic diversity of MHC genes found in this and other vertebrates. These MHC disassortative mating preferences are completely consistent with the conventional view that pathogen-driven MHC heterozygote advantage operates on MHC genes. This is because such matings preferentially produce MHC-heterozygours progeny, which could enjoy enhanced disease resistance. However, such matings could also function to avoid genome-wide inbreeding. To discriminate between these two hypotheses we measured the fitness consequences of both experimentally manipulated levels of inbreeding and MHC homozygosity and heterozygosity in semi-natural populations of wild-derived house mice. We were able to measure a fitness decline associated with inbreeding, but were unable to detect fitness declines associated with MHC homozygosity. These data suggest that inbreeding avoidance may be the most important function of MHC-based mating preferences and therefore the fundamental selective force diversifying MHC genes in species with such mating patterns. Although controversial, this conclusion is consistent with the majority of the data from the inbreeding and immunological literature.

C. J. Manning

Papers

The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test.