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      Female house sparrows "count on" male genes: experimental evidence for MHC-dependent mate preference in birds

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          Abstract

          Background

          Females can potentially assess the quality of potential mates using their secondary sexual traits, and obtain "good genes" that increase offspring fitness. Another potential indirect benefit from mating preferences is genetic compatibility, which does not require extravagant or viability indicator traits. Several studies with mammals and fish indicate that the genes of the major histocompatibility complex (MHC) influence olfactory cues and mating preferences, and such preferences confer genetic benefits to offspring. We investigated whether individual MHC diversity (class I) influences mating preferences in house sparrows ( Passer domesticus).

          Results

          Overall, we found no evidence that females preferred males with high individual MHC diversity. Yet, when we considered individual MHC allelic diversity of the females, we found that females with a low number of alleles were most attracted to males carrying a high number of MHC alleles, which might reflect a mating-up preference by allele counting.

          Conclusions

          This is the first experimental evidence for MHC-dependent mating preferences in an avian species to our knowledge. Our findings raise questions about the underlying mechanisms through which birds discriminate individual MHC diversity among conspecifics, and they suggest a novel mechanism through which mating preferences might promote the evolution of MHC polymorphisms and generate positive selection for duplicated MHC loci.

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          Most cited references61

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          MHC heterozygosity confers a selective advantage against multiple-strain infections.

          Genetic heterozygosity is thought to enhance resistance of hosts to infectious diseases, but few tests of this idea exist. In particular, heterozygosity at the MHC, the highly polymorphic loci that control immunological recognition of pathogens, is suspected to confer a selective advantage by enhancing resistance to infectious diseases (the "heterozygote advantage" hypothesis). To test this hypothesis, we released mice into large population enclosures and challenged them with multiple strains of Salmonella and one of Listeria. We found that during Salmonella infections with three avirulent strains, MHC heterozygotes had greater survival and weight than homozygotes (unlike sham controls), and they were more likely to clear chronic Salmonella infection than homozygotes. In laboratory experiments, we found that MHC heterozygosity enhanced the clearance of multiple-strain Salmonella infections. Yet, contrary to what is widely assumed, the benefits of heterozygosity were due to resistance being dominant rather than overdominant, i.e., heterozygotes were more resistant than the average of parental homozygotes, but they were not more resistant than both. The fact that MHC heterozygotes were more resistant to infection and had higher fitness than homozygotes provides a functional explanation for MHC-disassortative mating preferences.
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            Sexual selection and condition-dependent mate preferences.

            The last decade has witnessed considerable theoretical and empirical investigation of how male sexual ornaments evolve. This strong male-biased perspective has resulted in the relative neglect of variation in female mate preferences and its consequences for ornament evolution. As sexual selection is a co-evolutionary process between males and females, ignoring variation in females overlooks a key aspect of this process. Here, we review the empirical evidence that female mate preferences, like male ornaments, are condition dependent. We show accumulating support for the hypothesis that high quality females show the strongest mate preference. Nonetheless, this is still an infant field, and we highlight areas in need of more research, both theoretical and empirical. We also examine some of the wider implications of condition-dependent mating decisions and their effect on the strength of sexual selection.
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              The Evolution of Mating Preferences and Major Histocompatibility Complex Genes

              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 escape immune recognition (the Red Queen hypothesis). Such parasites are suspected to drive MHC diversity through rare-allele advantage. Thus, the two forms of parasite-mediated selection thought to drive MHC diversity, heterozygote and rare-allele advantage, will also favor MHC-dependent mating preferences. Finally, MHC-dependent mating preferences may also function to avoid inbreeding; a hypothesis consistent with other evidence that MHC genes play a role in kin recognition.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2011
                14 February 2011
                : 11
                : 44
                Affiliations
                [1 ]Konrad Lorenz Institute for Ethology, Austrian Academy of Sciences, Austria
                [2 ]Konrad Lorenz Institute for Ethology, Department of Integrative Biology and Evolution, University of Veterinary Medicine Vienna, Savoyenstrasse 1a, 1160 Vienna, Austria
                [3 ]UMR 7625 Ecologie & Evolution, Université Pierre et Marie Curie UPMC, CNRS ENS AgroParisTech, 7 quai Saint Bernard (case 237), F-75252 Paris Cedex 05, France
                Article
                1471-2148-11-44
                10.1186/1471-2148-11-44
                3044665
                21320306
                2aa88852-5077-4665-bbc9-2c2eb01573c3
                Copyright ©2011 Griggio et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 September 2010
                : 14 February 2011
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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