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.
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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)