Temporal variation of heterozygosity-based assortative mating and related benefits in a lesser kestrel population.

Heterozygosity as a target of mate choice has received much attention in recent years and there is growing evidence supporting its role in the evolution of mate preferences. In this study we analyse mating patterns in relation to heterozygosity in a lesser kestrel (Falco naumanni) population intensively monitored over six study years (2002-2007). The magnitude of heterozygosity-based assortative mating varied over time, being particularly patent in the last study years (2006, 2007). We have found evidence that this mating pattern entails both direct and indirect-genetic benefits. Clutch size increased with female heterozygosity and more heterozygous males raised a higher number of fledglings particularly in those years when the strength of the heterozygosity-based assortative mating was markedly higher. In the last study year, parent-offspring correlation of heterozygosity was stronger and higher than the expected if individuals would have randomly mated with respect to heterozygosity. Overall, our results offer empirical support to the heterozygous mate hypothesis of sexual selection but suggest that genetic diversity may act as a temporally variable target for mate choice.

Ortego J ，Calabuig G ，Bonal R ，Muñoz A ，Aparicio JM ，Cordero PJ ... -  《-》

Mate choice evolution, dominance effects, and the maintenance of genetic variation.

Female mate choice influences the maintenance of genetic variation by altering the mating success of males with different genotypes. The evolution of preferences themselves, on the other hand, depends on genetic variation present in the population. Few models have tracked this feedback between a choice gene and its effects on genetic variation, in particular when genes that determine offspring viability and attractiveness have dominance effects. Here we build a population genetic model that allows comparing the evolution of various choice rules in a single framework. We first consider preferences for good genes and show that focused preferences for homozygotes evolve more easily than broad preferences, which allow heterozygous males high mating success too. This occurs despite better maintenance of genetic diversity in the latter scenario, and we discuss why empirical findings of superior mating success of heterozygous males consequently do not immediately lead to a better understanding of the lek paradox. Our results thus suggest that the mechanisms that help maintain genetic diversity also have a flipside of making female choice an inaccurate means of producing the desired kind of offspring. We then consider preferences for heterozygosity per se, and show that these evolve only under very special conditions. Choice for compatible genotypes can evolve but its selective advantage diminishes quickly due to frequency-dependent selection. Finally, we show that our model reproduces earlier results on selfing, when the female choice strategy produces assortative mating. Overall, our model indicates that various forms of heterozygote-favouring (or variable) female choice pose a problem for the theory of sexual ornamentation based on indirect benefits, rather than a solution.

Lehmann L ，Keller LF ，Kokko H 《JOURNAL OF THEORETICAL BIOLOGY》

Egg production and individual genetic diversity in lesser kestrels.

Fecundity is an important component of individual fitness and has major consequences on population dynamics. Despite this, the influence of individual genetic variability on egg production traits is poorly known. Here, we use two microsatellite-based measures, homozygosity by loci and internal relatedness, to analyse the influence of female genotypic variation at 11 highly variable microsatellite loci on both clutch size and egg volume in a wild population of lesser kestrels (Falco naumanni). Genetic diversity was associated with clutch size, with more heterozygous females laying larger clutches, and this effect was statistically independent of other nongenetic variables such as female age and laying date, which were also associated with fecundity in this species. However, egg volume was not affected by female heterozygosity, confirming previous studies from pedigree-based breeding experiments which suggest that this trait is scarcely subjected to inbreeding depression. Finally, we explored whether the association between heterozygosity and clutch size was due to a genome-wide effect (general effect) or to single locus heterozygosity (local effect). Two loci showed a stronger influence but the correlation was not fully explained by these two loci alone, suggesting that a main general effect underlies the association observed. Overall, our results underscore the importance of individual genetic variation for egg production in wild bird populations, a fact that could have important implications for conservation research and provides insights into the study of clutch size evolution and genetic variability maintenance in natural populations.

Ortego J ，Calabuig G ，Cordero PJ ，Aparicio JM ... -  《MOLECULAR ECOLOGY》

Evolution of mate choice for genome-wide heterozygosity.

The extent to which indirect genetic benefits can drive the evolution of directional mating preferences for more ornamented mates, and the mechanisms that maintain such preferences without depleting genetic variance, remain key questions in evolutionary ecology. We used an individual-based genetic model to examine whether a directional preference for mates with higher genome-wide heterozygosity (H), and consequently greater ornamentation, could evolve and be maintained in the absence of direct fitness benefits of mate choice. We specifically considered finite populations of varying size and spatial genetic structure, in which parent-offspring resemblance in heterozygosity could provide an indirect benefit of mate choice. A directional preference for heterozygous mates evolved under broad conditions, even given a substantial direct cost of mate choice, low mutation rate, and stochastic variation in the link between individual heterozygosity and ornamentation. Furthermore, genetic variance was retained under directional sexual selection. Preference evolution was strongest in smaller populations, but weaker in populations with greater internal genetic structure in which restricted dispersal increased local inbreeding among offspring of neighboring females that all preferentially mated with the same male. These results suggest that directional preferences for heterozygous or outbred mates could evolve and be maintained in finite populations in the absence of direct fitness benefits, suggesting a novel resolution to the lek paradox.

Fromhage L ，Kokko H ，Reid JM 《-》

Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine.

Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.

Schmoll T ，Dietrich V ，Winkel W ，Epplen JT ，Schurr F ，Lubjuhn T ... -  《EVOLUTION》