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

BMC Evolutionary Biology, Jun 2009

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

Herv Mulard 0 1 2 3 Etienne Danchin 0 2 Sandra L Talbot 5 Andrew M Ramey 5 Scott A Hatch 5 Jol F White 0 1 2 Fabrice Helfenstein 4 Richard H Wagner 1 0 Laboratoire Evolution et Diversite Biologique , UMR 5174, Universite Paul Sabatier, 118 Route de Narbonne, 31962 Toulouse Cedex 9 , France 1 Konrad Lorenz Institute for Ethology, Austrian Academy of Sciences , Savoyenstrasse 1a, A- 1160 Vienna , Austria 2 Laboratoire Fonctionnement et Evolution des Systeme Ecologiques, CNRS-UMR 7103, Ecology Institute, Universite Pierre et Marie Curie-Paris 6 , 7 Quai St Bernard, 75005 Paris , France 3 Laboratoire d'Ecologie et de Neuro-Ethologie Sensorielles, Universite Jean Monnet , 23 Rue Paul Michelon, 42023 Saint-Etienne Cedex 03 , France 4 Evolutionary Ecology Group, Institute of Ecology and Evolution, University of Bern , Baltzerstrasse 6, 3012 Bern , Switzerland 5 U.S. Geological Survey, Alaska Science Center , 4210 University Drive, Anchorage, Alaska, 99508 , USA 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. - Background Numerous traits influence mate choice that may produce non-random mating patterns in many species. Although most studies have focused on morphological and behavioral traits [1-4]), there is rapidly growing evidence of multiple genetic criteria of mate choice (reviewed in [5,6]). For example, females might choose the most heterozygous males [7], which may increase the resistance of offspring to parasites [8,9]. Alternatively, females might choose males carrying alleles that are compatible with their own genotypes. The main driving forces of mate choice would then be to maintain equilibrium between co-adapted genes [10] or alternatively, to enhance the genetic variability of offspring [11-16]. In species with biparental care, both sexes should be choosy in selecting a mate [17,18]. Blomqvist et al. [14] reported that in socially monogamous shorebirds, both sexes obtained extra-pair fertilizations when mates were genetically similar. In blue tits (Parus caeruleus), females acquired extra-pair fertilizations that enhanced the heterozygosity and fitness of their offspring [19]. In superb starlings (Lamprotornis superbus), the benefits of extra-pair fertilizations may differ according to the genetic similarity of the extra-pair partner [20]. However, few studies have focused on the mating patterns in genetically monogamous species which lack extra-pair fertilizations to diminish the costs of pairing with a suboptimal mate. The black-legged kittiwake (Rissa tridactyla) is a long-lived, monogamous seabird with no extra-pair fertilizations [21] and high between-year repairing rates [22-25]. In this species, mate choice may thus profoundly affect reproductive success throughout an individual's lifetime. To examine whether mating patterns in kittiwakes are influenced by genetic criteria, we assessed individual heterozygosity and genetic similarity of mates with microsatellite markers. Our first aim was to examine three hypotheses of mating patterns driven by individual genotypes. Breeders may be paired with: (1) heterozygous mates ("preference of heterozygous mates" hypothesis; [15]), (2) genetically dissimilar mates, in order to increase the genetic variability of offspring ("genetic similarity avoidance" hypothesis; [14,26,27]), or (3) genetically similar mates, in order to preserve the link between locally co-adapted genes ("genetic similarity preference" hypothesis; [10,28]). According to Hypothesis 1, the most heterozygous mates are of better quality because they may provide direct benefits (e.g., better parental care) and/or indirect benefits in term of mo (...truncated)


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Hervé Mulard, Etienne Danchin, Sandra L Talbot, Andrew M Ramey, Scott A Hatch, Joël F White, Fabrice Helfenstein, Richard H Wagner. Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird, BMC Evolutionary Biology, 2009, pp. 147, 9, DOI: 10.1186/1471-2148-9-147