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      Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird

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          Abstract

          Background

          Evidence of multiple genetic criteria of mate choice is accumulating in numerous taxa. In many species, females have been shown to pair with genetically dissimilar mates or with extra-pair partners that are more genetically compatible than their social mates, thereby increasing their offsprings' heterozygosity which often correlates with offspring fitness. While most studies have focused on genetically promiscuous species, few studies have addressed genetically monogamous species, in which mate choice tends to be mutual.

          Results

          Here, we used microsatellite markers to assess individual global heterozygosity and genetic similarity of pairs in a socially and genetically monogamous seabird, the black-legged kittiwake Rissa tridactyla. We found that pairs were more genetically dissimilar than expected by chance. We also identified fitness costs of breeding with genetically similar partners: (i) genetic similarity of pairs was negatively correlated with the number of chicks hatched, and (ii) offspring heterozygosity was positively correlated with growth rate and survival.

          Conclusion

          These findings provide evidence that breeders in a genetically monogamous species may avoid the fitness costs of reproducing with a genetically similar mate. In such species that lack the opportunity to obtain extra-pair fertilizations, mate choice may therefore be under high selective pressure.

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          Most cited references78

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          Estimation of pairwise relatedness with molecular markers.

          Applications of quantitative genetics and conservation genetics often require measures of pairwise relationships between individuals, which, in the absence of known pedigree structure, can be estimated only by use of molecular markers. Here we introduce methods for the joint estimation of the two-gene and four-gene coefficients of relationship from data on codominant molecular markers in randomly mating populations. In a comparison with other published estimators of pairwise relatedness, we find these new "regression" estimators to be computationally simpler and to yield similar or lower sampling variances, particularly when many loci are used or when loci are hypervariable. Two examples are given in which the new estimators are applied to natural populations, one that reveals isolation-by-distance in an annual plant and the other that suggests a genetic basis for a coat color polymorphism in bears.
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            MHC-dependent mate preferences in humans.

            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.
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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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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2009
                30 June 2009
                : 9
                : 147
                Affiliations
                [1 ]Laboratoire Fonctionnement et Évolution des Système Écologiques, CNRS-UMR 7103, Ecology Institute, Université Pierre et Marie Curie-Paris 6, 7 Quai St Bernard, 75005 Paris, France
                [2 ]Konrad Lorenz Institute for Ethology, Austrian Academy of Sciences, Savoyenstrasse 1a, A-1160 Vienna, Austria
                [3 ]Laboratoire Évolution et Diversité Biologique, UMR 5174, Université Paul Sabatier, 118 Route de Narbonne, 31962 Toulouse Cedex 9, France
                [4 ]U.S. Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, Alaska, 99508, USA
                [5 ]Evolutionary Ecology Group, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerland
                [6 ]Laboratoire d'Écologie et de Neuro-Éthologie Sensorielles, Université Jean Monnet, 23 Rue Paul Michelon, 42023 Saint-Étienne Cedex 03, France
                Article
                1471-2148-9-147
                10.1186/1471-2148-9-147
                2709659
                19566922
                87c589dc-3fdf-4863-90b2-11adc337b143
                Copyright © 2009 Mulard 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
                : 15 January 2009
                : 30 June 2009
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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