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.
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 F ST 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. Electronic supplementary material The online version of this article (10.1186/s12862-019-1392-5) contains supplementary material, which is available to authorized users.
It has been suggested that adaptive evolution on ecological timescales shapes communities. However, adaptation among environments relies on isolation or large selection coefficients that exceed migration effects. This reliance is tempered if adaptation is polygenic-does not depend on one allele completely replacing another but instead requires small allele frequency changes at many loci. Thus, whether individuals can evolve adaptation to fine-scale habitat variation (for example, microhabitats) is not resolved. Here we analyze the genetic divergence of the teleost fish, Fundulus heteroclitus, among microhabitats that are <200 m apart in three separate saltmarshes using 4741 single-nucleotide polymorphisms (SNPs). Among these SNPs, 1.3-2.3% have large and highly significant differences among microhabitats (mean F=0.15; false discovery rate ⩽1%). The divergence among microhabitats for these outlier SNPs is larger than that among populations, exceeds neutral expectation and indicates surprising population structure among microhabitats. Thus, we suggest that polygenic selection is surprisingly effective in altering allele frequencies among many different SNPs that share similar biological functions in response to environmental and ecological differences over very small geographic distances. We acknowledge the evolutionary difficulty of large genetic divergence among well-connected habitats. Therefore, these studies are only the first step to discern whether natural selection is responsible and capable of effecting genetic divergence on such a fine scale.
Temperature changes affect metabolism on acute, acclamatory, and evolutionary time scales. To better understand temperature's affect on metabolism at these different time scales, we quantified cardiac oxidative phosphorylation (OxPhos) in three Fundulus taxa acclimated to 12 and 28°C and measured at three acute temperatures (12, 20, and 28°C). The Fundulus taxa (northern Maine and southern Georgia F. heteroclitus, and a sister taxa, F. grandis) were used to identify evolved changes in OxPhos. Cardiac OxPhos metabolism was quantified by measuring six traits: state 3 (ADP and substrate-dependent mitochondrial respiration); E state (uncoupled mitochondrial activity); complex I, II, and IV activities; and LEAK ratio. Acute temperature affected all OxPhos traits. Acclimation only significantly affected state 3 and LEAK ratio. Populations were significantly different for state 3. In addition to direct effects, there were significant interactions between acclimation and population for complex I and between population and acute temperature for state 3. Further analyses suggest that acclimation alters the acute temperature response for state 3, E state, and complexes I and II: at the low acclimation temperature, the acute response was dampened at low assay temperatures, and at the high acclimation temperature, the acute response was dampened at high assay temperatures. Closer examination of the data also suggests that differences in state 3 respiration and complex I activity between populations were greatest between fish acclimated to low temperatures when assayed at high temperatures, suggesting that differences between the populations become more apparent at the edges of their thermal range.
The oxidative phosphorylation (OxPhos) pathway is responsible for most aerobic ATP production and is the only metabolic pathway with proteins encoded by both nuclear and mitochondrial genomes. In studies examining mitonuclear interactions among distant populations within a species or across species, the interactions between these two genomes can affect metabolism, growth, and fitness, depending on the environment. However, there is little data on whether these interactions impact natural populations within a single species. In an admixed Fundulus heteroclitus population with northern and southern mitochondrial haplotypes, there are significant differences in allele frequencies associated with mitochondrial haplotype. In this study, we investigate how mitochondrial haplotype and any associated nuclear differences affect six OxPhos parameters within a population. The data demonstrate significant OxPhos functional differences between the two mitochondrial genotypes. These differences are most apparent when individuals are acclimated to high temperatures with the southern mitochondrial genotype having a large acute response and the northern mitochondrial genotype having little, if any acute response. Furthermore, acute temperature effects and the relative contribution of Complex I and II depend on acclimation temperature: when individuals are acclimated to 12°C, the relative contribution of Complex I increases with higher acute temperatures, whereas at 28°C acclimation, the relative contribution of Complex I is unaffected by acute temperature change. These data demonstrate a complex gene by environmental interaction affecting the OxPhos pathway.
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