To our knowledge, our work represents the first study carried in a natural fish population suggesting a causal link between mate choice, MHC variation and offspring fitness. We addressed this by manipulating mate choice and comparing MHC variability and parasite susceptibility between the progeny of wild salmon (able to mate freely) and hatchery-bred fish (deprived of the potential benefits of mate choice). The parasite we targeted (Anisakis
sp.) is a marine nematode commonly found in salmon (Bakke & Harris 1998
), which act as paratenic intermediate host. Screening of a marine (rather than of a freshwater) parasite minimized potential confounding effects due to possible differences in early rearing between hatchery and wild fish. Fish react to Anisakis
by producing apoptosis-inducing proteins in infected tissues (Jung et al. 2000
), suggesting that Anisakis
can seriously hamper fish health.
Salmonids do not show parental care, and since males provide only genes for the offspring, indirect genetic benefits may be particularly important in this family. Yet, despite numerous studies on MHC-mediated mate choice (reviewed in Jordan & Bruford 1998
; Penn 2002
), there is little evidence for MHC indirect genetic benefits. Females could benefit from choosing MHC-dissimilar males by increasing MHC diversity of their offspring—and thereby improving offspring immunocompetence (Apanius et al. 1997
)—or by decreasing the risks of inbreeding or maximizing genetic compatibility (Tregenza & Wedell 2000
). Strong homing behaviour (i.e. the ability to return to reproduce to the place of birth) should favour the recognition and avoidance of close mates, but a promiscuous mating system argues against a major role for inbreeding avoidance in the evolution of salmonid life histories (Consuegra & Garcia de Leaniz 2007
). On the other hand, evidence for the effect of MHC genotype on parasite resistance in the wild remains controversial (Sommer 2005
). Indeed, parasite loads in wild populations of three-spined stickleback seem to be unrelated to MHC genotype (Rauch et al. 2006
We found a much higher abundance of Anisakis
in the offspring of artificially crossed salmon than that of wild conspecifics, suggesting that in the absence of mate choice salmon may be more susceptible to parasitic infection. Although population levels of MHC genetic diversity were similar for wild and hatchery salmon, the progeny of free mating fish (but not those derived from artificial crosses) were more MHC dissimilar than would be expected by chance. We interpret this as evidence of disassortative mating in the wild, in line with recent work that suggests that the female salmonids may choose males on the basis of MHC dissimilarity (Landry et al. 2001
; Forsberg et al. 2007
). Moreover, those individuals resistant to Anisakis
infection had greater MHC dissimilarity than infected fish, strongly suggesting that the offspring of MHC disassortative matings might benefit from increased resistance to parasitic infection.
We failed to find any association between specific MHC alleles and parasite loads or between heterozygosity and increased parasite resistance. These findings are more consistent with compatible genes than with good genes scenarios, though both hypotheses may not be mutually exclusive (Pitcher & Neff 2006
; Reid 2007
). For example, conditions favouring mate choice for good genes may alternate with those favouring compatible genes, and some females may select mates for good genes while others may select for compatible genes. Furthermore, the relative importance of additive and non-additive effects on fitness may vary over the course of development (Wedekind et al. 2001
) and, in some mating systems, females may also accrue non-additive genetic benefits from directional mate choice (Reid 2007
We cannot completely disregard the possibility that differences in MHC dissimilarity between hatchery and wild fish might have been caused by non-random sampling of alleles in the hatchery broodstock or by differences in selective pressures during the first months of life. However, the number of different crosses carried out in the captive breeding programme was reasonably large and MHC heterozygosity and allelic richness were the same for hatchery and wild fish. Thus, differences in MHC dissimilarity are most probably due to the effects of mate choice and indicative of disassortative mating among wild fish. It is also unlikely that differences in parasite loads can be attributed to early hatchery rearing (rather than to mate choice), as fish can only become infected with Anisakis in the common marine phase during their second or third year of life. Differences in early rearing histories between hatchery and wild fish could have also resulted in temporal or spatial differences in patterns of marine migrations, and consequently in differential exposure to marine parasites. However, the significant association between MHC dissimilarity and resistance to Anisakis is also evident when hatchery fish are excluded from analysis, making this interpretation unlikely.
Field studies carried out in the wild are the only ones that can control for genotype×environment interactions, which are very common in fitness traits in salmonids (Garcia de Leaniz et al. 2007
), and may confound studies of mate choice and genetic quality (Neff & Pitcher 2005
). However, one inevitable shortcoming of natural studies is that mating preferences and indirect genetic benefits must necessarily be inferred from posterior analysis of offspring genotypes (e.g. Forsberg et al. 2007
). Here, we inferred MHC-mediated mate choice from the analysis of F1 genotypes among returning adults, which could have also reflected MHC-related mortality at any stage of development. We do not rule out the possibility of differential mortality of MHC genotypes, but this would not explain the observed differences in MHC dissimilarity between the progeny of hatchery and wild fish, or the random distribution of MHC alleles among the offspring of artificially bred salmon.
In conclusion, our results suggest that salmon choose mates on the basis of MHC dissimilarity and that the MHC dissimilarity (rather than heterozygosity or specific combinations of alleles) can make their offspring more resistant to parasite infection. We therefore provide some evidence for a link between disassortative mating and offspring benefits and support the idea that both natural and sexual selection shape the evolution of MHC genes. Although our results do not rule out the possibility of ‘MHC optimality’ (Wegner et al. 2003
), we did not specifically test for it as Atlantic salmon express only two MHC class II-α alleles.
There is ample evidence that artificially bred animals have lower fitness than wild conspecifics, and this is often attributed to domestication, reduced genetic variation or behavioural deficits (Lynch & O'Hely 2001
). Consequently, considerable efforts are made in captive breeding to make rearing conditions more ‘natural’ or maximize genetic variation. However, our study indicates that artificial breeding may significantly reduce offspring fitness simply through lack of mate choice, as shown recently by Pitcher & Neff (2007)
. This can have important implications for conservation programmes (including gene banking) and commercial farming alike, since artificial reproduction that negates sexual selection and mate choice may result in inherently inferior offspring, regardless of population size, rearing conditions or genetic diversity.