The mating patterns observed in this study strongly promote the idea of Mhc-related mate choice in birds. Mate choice in house sparrows proved to be based not only on the partners' allelic diversity at Mhc loci, but also on the number of shared Mhc alleles. As a result, males of low Mhc diversity that were too dissimilar from females at Mhc loci (i.e. no common alleles) were excluded from reproductive events. Moreover, Mhc diversity was positively correlated in both mating partners. Importantly, variation at neutral microsatellite markers did not influence reproductive decisions, suggesting that variation at Mhc loci per se may be driving mate choice in this population.
It is currently debated whether selection favours an intermediate or a maximum number of Mhc
alleles (Penn et al. 2002
; McClelland et al. 2003
; Hedrick 2004
; Wegner et al. 2004
). An optimum number of Mhc
alleles could be generated by a trade-off between selection for recognition of the largest antigenic peptide repertoire (Carrington et al. 1999
; Arkush et al. 2002
; Penn et al. 2002
; McClelland et al. 2003
), which favours more alleles, and selection to minimize the loss of T cell clones due to self-tolerance induction (Nowak et al. 1992
), which favours fewer. By excluding males that are too dissimilar (i.e. band-sharing=0), female house sparrows may prevent diversity from reaching detrimental levels in their offspring. Yet, by giving preference to mates with high allelic diversity, they may simultaneously endeavour to maximize the number of Mhc
alleles in their progeny.
Rejection of the most dissimilar males may, however, have a larger significance than just avoiding costs of unfavourable diversity at the Mhc
. Mating between highly divergent partners may disrupt local adaptations or co-adapted gene complexes (Hendry et al. 2000
) and produce offspring of lower fitness. Furthermore, intermediate levels of genomic divergence have been shown to be associated with higher reproductive success than more extreme levels of divergence (Neff 2004
). The optimal level of genomic divergence may hence vary according to whether it is more advantageous to produce higher-quality surviving inbreds despite the increased mortality of offspring.
were found to be significantly associated with each other. In a previous study involving this population of wild house sparrows, the allele a172
was found to be associated with higher resistance to infections with the most common local Plasmodium
strain, whereas none of the individuals that carried the a163
allele endured simultaneous infections with two strains of malaria parasites (Bonneaud et al. 2005
). We can easily speculate that rupture of this association of alleles would be selectively detrimental to the individual in terms of increased susceptibility to malaria infections. Co-adapted genes therefore exist in this population and probably undergo both parasite-mediated selection and reproductive selection.
Analyses of relatedness at neutral microsatellite loci showed that this population was outbred. In addition, mate choice was found to be based uniquely on Mhc genotypes, as females were not more or less closely related to the subset of males they paired with. Females only had 0.03% chances of pairing with a male carrying an identical combination of microsatellite alleles and 8% chances of pairing with a completely different male, so the absence of microsatellite-based reproductive preferences may be explained by a lack of inbreeding or outbreeding risks at neutral loci.
Our study reveals that females favoured males of comparable Mhc
diversity and with higher numbers of matching alleles than found at random. It is fundamental to point out that females did not select males with identical Mhc
genotypes, but rather excluded males with whom they shared no alleles. Hence our findings do not contradict previous work reporting avoidance of Mhc
-similar mates (Yamazaki et al. 1976
; Potts et al. 1991
; Freeman-Gallant et al. 2003
). Most experimental assessments of mate choice have examined female preference between males of Mhc
genotypes identical or different from their own. Yet, recent evidence suggests preference for mates with small or intermediate numbers of matching Mhc
alleles rather than for mates with no or all matching alleles (Jacob et al. 2002
). In this outbred population, the probability of pairing with a male of identical Mhc
genotype was extremely low (0.3%), whereas the chance of randomly pairing with a male carrying a completely different set of Mhc
alleles (i.e. band-sharing=0) was 54%. A biased decision may allow females to control the number of Mhc
alleles in their progeny and their overall level of genomic divergence, while still maximizing the number of Mhc
alleles by favouring the most diverse males.
An underlying assumption to Mhc
-based mate choice is that Mhc
genotypes can be predicted by phenotypic traits used as cues by choosy partners. The direct implications of Mhc
genes in fighting off diseases make obvious the links between Mhc
genotypes and condition-dependent traits (Zelano & Edwards 2002
). We failed to show any significant correlation between Mhc
genotypes and body mass or tarsus length in males and females, or expression of a male secondary sexual trait (badge size). In the same way, coefficients of spatial autocorrelation did not indicate any particular structuring of males, females or pairs as a function of their number of Mhc
alleles. Studies on Mhc
-based mate choice in mammals and fish indicate that olfactory cues are generally used to discriminate among Mhc
genotypes (Brown & Eklund 1994
; Reusch et al. 2001
). Because birds are commonly thought to be anosmatic, targets of sexual selection usually involve visual signals. Yet recent experimental work on different bird orders has revealed unsuspected abilities to discriminate between the odours of conspecifics and between those of aromatic plants (Petit et al. 2002
; Hagelin et al. 2003
; Bonadonna & Nevitt 2004
). Association between the Mhc
, odours, and mating preferences in birds is a promising question that awaits further exploration.