Local heterozygosity-fitness correlations with global positive effects on fitness in threespine stickleback

The complex interactions between genetic diversity and evolution have important implications in many biological areas including conservation, speciation, and mate choice. A common way to study these interactions is to look at heterozygosity-fitness correlations (HFCs). Until recently, HFCs based on noncoding markers were believed to result primarily from global inbreeding effects. However, accumulating theoretical and empirical evidence shows that HFCs may often result from genes being linked to the markers used (local effect). Moreover, local effect HFCs could differ from global inbreeding effects in their direction and occurrence. Consequently, the investigation of the structure and consequences of local HFCs is emerging as a new important goal in evolutionary biology. In this study of a wild threespine stickleback (Gasterosteus aculeatus) population, we first tested the presence of significant positive or negative local effects of heterozygosity at 30 microsatellites loci on five fitness components: survival, mating success, territoriality, length, and body condition. Then, we evaluated the direction and shape of total impact of local HFCs, and estimated the magnitude of the impacts on fitness using regression coefficients and selection differentials. We found that multilocus heterozygosity was not a reliable estimator of individual inbreeding coefficient, which supported the relevance of single-locus based analyses. Highly significant and temporally stable local HFCs were observed. These were mainly positive, but negative effects of heterozygosity were also found. Strong and opposite effects of heterozygosity are probably present in many populations, but may be blurred in HFC analyses looking for global effects only. In this population, both negative and positive HFCs are apparently driving mate preference by females, which is likely to contribute to the maintenance of both additive and nonadditive genetic variance.