Evolved genetic and phenotypic differences due to mitochondrial-nuclear interactions.

The oxidative phosphorylation (OxPhos) pathway is responsible for most aerobic ATP production and is the only pathway with both nuclear and mitochondrial encoded proteins. The importance of the interactions between these two genomes has recently received more attention because of their potential evolutionary effects and how they may affect human health and disease. In many different organisms, healthy nuclear and mitochondrial genome hybrids between species or among distant populations within a species affect fitness and OxPhos functions. However, what is less understood is whether these interactions impact individuals within a single natural population. The significance of this impact depends on the strength of selection for mito-nuclear interactions. We examined whether mito-nuclear interactions alter allele frequencies for ~11,000 nuclear SNPs within a single, natural Fundulus heteroclitus population containing two divergent mitochondrial haplotypes (mt-haplotypes). Between the two mt-haplotypes, there are significant nuclear allele frequency differences for 349 SNPs with a p-value of 1% (236 with 10% FDR). Unlike the rest of the genome, these 349 outlier SNPs form two groups associated with each mt-haplotype, with a minority of individuals having mixed ancestry. We use this mixed ancestry in combination with mt-haplotype as a polygenic factor to explain a significant fraction of the individual OxPhos variation. These data suggest that mito-nuclear interactions affect cardiac OxPhos function. The 349 outlier SNPs occur in genes involved in regulating metabolic processes but are not directly associated with the 79 nuclear OxPhos proteins. Therefore, we postulate that the evolution of mito-nuclear interactions affects OxPhos function by acting upstream of OxPhos.

Population genomics of rapid evolution in natural populations: polygenic selection in response to power station thermal effluents.

BACKGROUND: Examples of rapid evolution are common in nature but difficult to account for with the standard population genetic model of adaptation. Instead, selection from the standing genetic variation permits rapid adaptation via soft sweeps or polygenic adaptation. Empirical evidence of this process in nature is currently limited but accumulating. RESULTS: We provide genome-wide analyses of rapid evolution in Fundulus heteroclitus populations subjected to recently elevated temperatures due to coastal power station thermal effluents using 5449 SNPs across two effluent-affected and four reference populations. Bayesian and multivariate analyses of population genomic structure reveal a substantial portion of genetic variation that is most parsimoniously explained by selection at the site of thermal effluents. An FST outlier approach in conjunction with additional conservative requirements identify significant allele frequency differentiation that exceeds neutral expectations among exposed and closely related reference populations. Genomic variation patterns near these candidate loci reveal that individuals living near thermal effluents have rapidly evolved from the standing genetic variation through small allele frequency changes at many loci in a pattern consistent with polygenic selection on the standing genetic variation. CONCLUSIONS: While the ultimate trajectory of selection in these populations is unknown and we survey only a minority of genomic loci, our findings suggest that polygenic models of adaptation may play important roles in large, natural populations experiencing recent selection due to environmental changes that cause broad physiological impacts.

Phenotypic plasticity in gene expression contributes to divergence of locally adapted populations of Fundulus heteroclitus.

We examine the interaction between phenotypic plasticity and evolutionary adaptation using muscle gene expression levels among populations of the fish Fundulus heteroclitus acclimated to three temperatures. Our analysis reveals shared patterns of phenotypic plasticity due to thermal acclimation as well as non-neutral patterns of variation among populations adapted to different thermal environments. For the majority of significant differences in gene expression levels, phenotypic plasticity and adaptation operate on different suites of genes. The subset of genes that demonstrate both adaptive differences and phenotypic plasticity, however, exhibit countergradient variation of expression. Thus, expression differences among populations counteract environmental effects, reducing the phenotypic differentiation between populations. Finally, gene-by-environment interactions among genes with non-neutral patterns of expression suggest that the penetrance of adaptive variation depends on the environmental conditions experienced by the individual.

A single generation in the wild increases fitness for descendants of hatchery-origin Chinook salmon (Oncorhynchus tshawytscha).

Reintroduction is an important tool for the recovery of imperiled species. For threatened Pacific salmonids (Oncorhynchus spp.) species, hatchery-origin (HOR) individuals from a nearby source are often used to reestablish populations in vacant, historically occupied habitat. However, this approach is challenged by the relatively low reproductive success that HOR Pacific salmonids experience when they spawn in the wild, relative to their natural-origin (NOR) counterparts. In this study, we used genetic parentage analysis to compare the reproductive success of three groups of adult Chinook salmon (Oncorhynchus tshawytscha) reintroduced above Cougar Dam on the South Fork McKenzie River, Oregon: HOR Chinook salmon from an integrated stock; first-generation, wild-born descendants (hereafter F 1s) of Chinook salmon produced at the same hatchery; and NOR Chinook salmon that are presumed to have been produced below the dam, on the mainstem McKenzie River, or elsewhere and volitionally entered a trap below Cougar Dam. We found that F 1s produced nearly as many adult offspring as NORs, and 1.8-fold more adult offspring than HORs. This result suggests that, for the South Fork McKenzie reintroduction program, a single generation in the wild increases fitness for the descendants of HOR Chinook salmon. Although these results are encouraging, care must be taken before extrapolating our results to other systems.