Abstract
Under inbreeding, heterozygosity at neutral genetic markers is likely to reflect genome-wide heterozygosity and, thus, is expected to correlate with fitness. There is, however, growing evidence that some of heterozygosity-fitness correlations (HFCs) can be explained by ‘local effects’, where noncoding loci are at linkage disequilibrium with functional genes. The aim of this study was to investigate correlations between heterozygosity at seven microsatellite loci and two fitness-related traits, nestling growth rate and nutritional condition, in a recently bottlenecked population of great cormorant Phalacrocorax carbo sinensis. We found that heterozygosity was positively associated with both nestling traits at the between-brood level, but the individual (within-brood) effects of heterozygosity were non-significant. We also found that only one locus per trait was primarily responsible for the significant multi-locus HFCs, suggesting a linkage disequilibrium with non-identified functional loci. The results give support for ‘local effect’ hypothesis, confirming that HFCs may not only be interpreted as evidence of inbreeding and that genetic associations between functional and selectively neutral markers could be much more common in natural populations than previously thought.
Highlights
Genotype-phenotype associations are often complex and difficult to disentangle, but the impact of individual genetic variation on phenotypic quality and fitness has long been recognized as an important evolutionary mechanism
To test whether the heterozygosity-fitness correlations (HFCs) recorded at the between-nest level for each of fitness-related traits can be explained with the local effect hypothesis we compared a model incorporating specific heterozygosity effects separately for each locus (m2) with a model of multi-locus heterozygosity calculated across all loci (m1, following Szulkin et al 2010)
While we failed to find any significant difference in the variance explained by both models for nestling growth rate (F6,149 = 0.87, p = 0.52), there was a strong support for a local effect of heterozygosity acting on chick nutritional condition, as the model with single-locus effects
Summary
Genotype-phenotype associations are often complex and difficult to disentangle, but the impact of individual genetic variation on phenotypic quality and fitness has long been recognized as an important evolutionary mechanism. Heterozygosity at neutrally selected loci has been assumed to correlate with fitness only in inbred populations, where it is expected to reflect genome-wide heterozygosity, which in turn should correlate with individual inbreeding coefficient (Coulson et al 1998; Slate et al 2000) This mechanism is recognized as a ‘general effect’ of heterozygosity and it was initially suggested to explain a large majority of all HFCs reported for noncoding markers. This interpretation was recently challenged by studies showing a weak association between the inbreeding coefficient and heterozygosity measured across a large number of neutrally selected loci (Balloux et al 2004; Markert et al 2004; Slate et al 2004). It seems that these specific conditions rarely occur in the wild and, they are unlikely to explain most of the HFCs reported in empirical studies on vertebrates (Pemberton 2004)
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