Evolutionary implications of mitochondrial genetic variation: mitochondrial genetic effects on OXPHOS respiration and mitochondrial quantity change with age and sex in fruit flies

The ancient acquisition of the mitochondrion into the ancestor of modern‐day eukaryotes is thought to have been pivotal in facilitating the evolution of complex life. Mitochondria retain their own diminutive genome, with mitochondrial genes encoding core subunits involved in oxidative phosphorylation. Traditionally, it was assumed that there was little scope for genetic variation to accumulate and be maintained within the mitochondrial genome. However, in the past decade, mitochondrial genetic variation has been routinely tied to the expression of life‐history traits such as fertility, development and longevity. To examine whether these broad‐scale effects on life‐history trait expression might ultimately find their root in mitochondrially mediated effects on core bioenergetic function, we measured the effects of genetic variation across twelve different mitochondrial haplotypes on respiratory capacity and mitochondrial quantity in the fruit fly, Drosophila melanogaster. We used strains of flies that differed only in their mitochondrial haplotype, and tested each sex separately at two different adult ages. Mitochondrial haplotypes affected both respiratory capacity and mitochondrial quantity. However, these effects were highly context‐dependent, with the genetic effects contingent on both the sex and the age of the flies. These sex‐ and age‐specific genetic effects are likely to resonate across the entire organismal life‐history, providing insights into how mitochondrial genetic variation may contribute to sex‐specific trajectories of life‐history evolution.     

Evolutionary potential of hidden genetic variation

The ability of a population to respond to natural or artificial selection pressures is determined by the genetic architecture of the selected trait. It is now widely acknowledged that a substantial part of genetic variability can be buffered or released as the result of complex genetic interactions. However, the impact of hidden genetic diversity on phenotypic evolution is still not clear. Here, we argue that a common term to describe the impact of hidden genetic variation on phenotypic change is needed and will help to provide new insights into the contribution of different components of genetic architectures to the evolvability of a character. We introduce the 'genetic charge' concept, to describe how the architecture of a trait can be 'charged' with potential for evolutionary change that can later be 'discharged' in response to selection.     

Evolutionary genetics: the nature of hidden genetic variation unveiled

It has long been known that wild-type phenotypes harbor considerable amounts of ‘hidden’ genetic variation. A new study has mapped this variation at the nucleotide level and revealed some unexpected properties.     

Evolutionary response when selection and genetic variation covary across environments

Although models of evolution usually assume that the strength of selection on a trait and the expression of genetic variation in that trait are independent, whenever the same ecological factor impacts both parameters, a correlation between the two may arise that accelerates trait evolution in some environments and slows it in others. Here, we address the evolutionary consequences and ecological causes of a correlation between selection and expressed genetic variation. Using a simple analytical model, we show that the correlation has a modest effect on the mean evolutionary response and a large effect on its variance, increasing among‐population or among‐generation variation in the response when positive, and diminishing variation when negative. We performed a literature review to identify the ecological factors that influence selection and expressed genetic variation across traits. We found that some factors – temperature and competition – are unlikely to generate the correlation because they affected one parameter more than the other, and identified others – most notably, environmental novelty – that merit further investigation because little is known about their impact on one of the two parameters. We argue that the correlation between selection and genetic variation deserves attention alongside other factors that promote or constrain evolution in heterogeneous landscapes.     

Conservation versus variation of dinucleotide frequencies across genomes: Evolutionary implications

Background  

In order to find traits or evolutionary relics of the primordial genome (the most primitive nucleic acid genome for earth's life) remained in modern genomes, we have studied the characteristics of dinucleotide frequencies across genomes. As the longer a sequence is, the more probable it would be modified during genome evolution. For that reason, short nucleotide sequences, especially dinucleotides, would have considerable chances to be intact during billions of years of evolution. Consequently, conservation of the genomic profiles of the frequencies of dinucleotides across modern genomes may exist and would be an evolutionary relic of the primordial genome.     

Post-glacial partitioning of mitochondrial genetic variation in the field vole

Genetic markers are often used to examine population history. There is considerable debate about the behaviour of molecular clock rates around the population-species transition. Nevertheless, appropriate calibration is critical to any inference regarding the absolute timing and scale of demographic changes. Here, we use a mitochondrial cytochrome b gene genealogy, based entirely on modern sequences and calibrated from recent geophysical events, to date the post-glacial expansion of the Eurasian field vole (Microtus agrestis), a widespread temperate mammal species. The phylogeographic structure reflects the subsequent expansion of populations that went through bottlenecks at the time of the Younger Dryas (ca 12,000 years BP) rather than the Last Glacial Maximum (LGM, ca 24,000 years BP), which is usually seen as the time when present-day patterns were determined. The nucleotide substitution rate that was estimated here, ca 4 × 10(-7) substitutions/site/year, remains extremely high throughout the relevant time frame. Calibration with similarly high population-based substitution rates, rather than long-term rates derived from species divergence times, will show that post-LGM climatic events generated current phylogeographic structure in many other organisms from temperate latitudes.     

Evolutionary rate variation at multiple levels of biological organization in plant mitochondrial DNA

We examined patterns of mitochondrial polymorphism and divergence in the angiosperm genus Silene and found substantial variation in evolutionary rates among species and among lineages within species. Moreover, we found corresponding differences in the amount of polymorphism within species. We argue that, along with our earlier findings of rate variation among genes, these patterns of rate heterogeneity at multiple phylogenetic scales are most likely explained by differences in underlying mutation rates. In contrast, no rate variation was detected in nuclear or chloroplast loci. We conclude that mutation rate heterogeneity is a characteristic of plant mitochondrial sequence evolution at multiple biological scales and may be a crucial determinant of how much polymorphism is maintained within species. These dramatic patterns of variation raise intriguing questions about the mechanisms driving and maintaining mutation rate heterogeneity in plant mitochondrial genomes. Additionally, they should alter our interpretation of many common phylogenetic and population genetic analyses.     

Evolutionary determinants of genetic variation in susceptibility to infectious diseases in humans

Although genetic variation among humans in their susceptibility to infectious diseases has long been appreciated, little focus has been devoted to identifying patterns in levels of variation in susceptibility to different diseases. Levels of genetic variation in susceptibility associated with 40 human infectious diseases were assessed by a survey of studies on both pedigree-based quantitative variation, as well as studies on different classes of marker alleles. These estimates were correlated with pathogen traits, epidemiological characteristics, and effectiveness of the human immune response. The strongest predictors of levels of genetic variation in susceptibility were disease characteristics negatively associated with immune effectiveness. High levels of genetic variation were associated with diseases with long infectious periods and for which vaccine development attempts have been unsuccessful. These findings are consistent with predictions based on theoretical models incorporating fitness costs associated with the different types of resistance mechanisms. An appreciation of these observed patterns will be a valuable tool in directing future research given that genetic variation in disease susceptibility has large implications for vaccine development and epidemiology.     

Evolutionary rates for multivariate traits: the role of selection and genetic variation

A fundamental question in evolutionary biology is the relative importance of selection and genetic architecture in determining evolutionary rates. Adaptive evolution can be described by the multivariate breeders'' equation (), which predicts evolutionary change for a suite of phenotypic traits () as a product of directional selection acting on them (β) and the genetic variance–covariance matrix for those traits (G). Despite being empirically challenging to estimate, there are enough published estimates of G and β to allow for synthesis of general patterns across species. We use published estimates to test the hypotheses that there are systematic differences in the rate of evolution among trait types, and that these differences are, in part, due to genetic architecture. We find some evidence that sexually selected traits exhibit faster rates of evolution compared with life-history or morphological traits. This difference does not appear to be related to stronger selection on sexually selected traits. Using numerous proposed approaches to quantifying the shape, size and structure of G, we examine how these parameters relate to one another, and how they vary among taxonomic and trait groupings. Despite considerable variation, they do not explain the observed differences in evolutionary rates.     

Evolutionary and genetic analyses of mitochondrial translation initiation factors identify the missing mitochondrial IF3 in S. cerevisiae

Mitochondrial translation is essentially bacteria-like, reflecting the bacterial endosymbiotic ancestry of the eukaryotic organelle. However, unlike the translation system of its bacterial ancestors, mitochondrial translation is limited to just a few mRNAs, mainly coding for components of the respiratory complex. The classical bacterial initiation factors (IFs) IF1, IF2 and IF3 are universal in bacteria, but only IF2 is universal in mitochondria (mIF2). We analyse the distribution of mitochondrial translation initiation factors and their sequence features, given two well-propagated claims: first, a sequence insertion in mitochondrial IF2 (mIF2) compensates for the universal lack of IF1 in mitochondria, and secondly, no homologue of mitochondrial IF3 (mIF3) is identifiable in Saccharomyces cerevisiae. Our comparative sequence analysis shows that, in fact, the mIF2 insertion is highly variable and restricted in length and primary sequence conservation to vertebrates, while phylogenetic and in vivo complementation analyses reveal that an uncharacterized S. cerevisiae mitochondrial protein currently named Aim23p is a bona fide evolutionary and functional orthologue of mIF3. Our results highlight the lineage-specific nature of mitochondrial translation and emphasise that comparative analyses among diverse taxa are essential for understanding whether generalizations from model organisms can be made across eukaryotes.     

Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease

Mitochondrial ribosomes comprise the most diverse group of ribosomes known. The mammalian mitochondrial ribosomes (55S) differ unexpectedly from bacterial (70S) and cytoplasmic ribosomes (80S), as well as other kinds of mitochondrial ribosomes. The bovine mitochondrial ribosome has been developed as a model system for the study of human mitochondrial ribosomes to address several questions related to the structure, function, biosynthesis and evolution of these interesting ribosomes. Bovine mitochondrial ribosomal proteins (MRPs) from each subunit have been identified and characterized with respect to individuality and electrophoretic properties, amino acid sequence, topographic disposition, RNA binding properties, evolutionary relationships and reaction with affinity probes of ribosomal functional domains. Several distinctive properties of these ribosomes are being elucidated, including their antibiotic susceptibility and composition. Mammalian mitochondrial ribosomes lack several of the major RNA stem structures of bacterial ribosomes but they contain a correspondingly higher protein content (as many as 80 proteins), suggesting a model where proteins have replaced RNA structural elements during the evolution of these ribosomes. Despite their lower RNA content they are physically larger than bacterial ribosomes, because of the 'extra' proteins they contain. The extra proteins in mitochondrial ribosomes are 'new' in the sense that they are not homologous to proteins in bacterial or cytoplasmic ribosomes. Some of the new proteins appear to be bifunctional. All of the mammalian MRPs are encoded in nuclear genes (a separate set from those encoding cytoplasmic ribosomal proteins) which are evolving more rapidly than those encoding cytoplasmic ribosomal proteins. The MRPs are imported into mitochondria where they assemble coordinately with mitochondrially transcribed rRNAs into ribosomes that are responsible for translating the 13 mRNAs for essential proteins of the oxidative phosphorylation system. Interest is growing in the structure, organization, chromosomal location and expression of genes for human MRPs. Proteins which are essential for mitoribosome function are candidates for involvement in human genetic disease.     

Evolutionary ecology of Datura stramonium: genetic variation and costs for tolerance to defoliation

The incorporation of plant tolerance after damage as a new alternative to cope with herbivory, as opposed to resistance, opened new avenues for our understanding of coevolution between plants and herbivores. Although genetic variation on tolerance to defoliation has been detected in some species, few studies have been undertaken with nonagricultural species. In this study, we explore in the annual weed Datura stramonium the existence of genetic variation for tolerance and fitness costs of tolerance. To determine which fitness-related trait was responsible for possible differences in tolerance, growth rate, total flower and fruit production, and the number of seeds per fruit were recorded. Inbred line replicates of D. stramonium from a population of Mexico City were exposed to four defoliation levels (0%, 10%, 30%, and 70%). Our results from a greenhouse experiment using controlled genetic material (inbred lines) indicated that significant genetic variation for tolerance was detected across defoliation environments. Defoliation reduced plant fitness from 15% to 25% in the highest levels of defoliation. Differences on tolerance among inbred lines were accounted by a differential reduction in the proportion of matured fruits across defoliation levels (up to 20%). Within defoliation levels, significant genetic variation in plant fitness suggests that tolerance could be selected. The correlation between fitness values of inbred lines in two environments (with and without damage) was positive (rg = 0.77), but not significant, suggesting absence of fitness costs for tolerance. The finding of genetic variation on tolerance might be either due to differences among inbred lines in their capability to overcome foliar damage through compensation or due to costs incurred by inducing secondary metabolites. Our results indicate the potential for norms of reaction to be selected under a gradient of herbivory pressure and highlights the importance of dissecting induced from compensatory responses when searching for potential causes of genetic variation on tolerance.     

Ecosystem implications of genetic variation in water-use of a dominant riparian tree

Genetic variation in dominant species can affect plant and ecosystem functions in natural systems through multiple pathways. Our study focuses on how genetic variation in a dominant riparian tree (Populus fremontii, P. angustifolia and their natural F₁ and backcross hybrids) affects whole-tree water use, and its potential ecosystem implications. Three major patterns were found. First, in a 12-year-old common garden with trees of known genetic makeup, hybrids had elevated daily integrated leaf-specific transpiration (E_tl ; P=0.013) and average canopy conductance (G_c ; P=0.037), with both E_tl and G_c ~30% higher in hybrid cross types than parental types. Second, ¹³C values of leaves from these same trees were significantly more negative in hybrids (P=0.004), and backcross hybrids had significantly more negative values than all other F₁ hybrid and parental types (P <0.001). Third, in the wild, a similar pattern was found in leaf ¹³C values where both hybrid cross types had the lowest values (P <0.001) and backcross hybrids had lower ¹³C values than any other tree type (P <0.001). Our findings have two important implications: (1) the existence of a consistent genetic difference in whole-tree physiology suggests that whole-tree gas and water exchange could be another pathway through which genes could affect ecosystems; and (2) such studies are important because they seek to quantify the genetic variation that exists in basic physiological processes—such knowledge could ultimately place ecosystem studies within a genetic framework.     

Evolutionary tinkering with mitochondrial nucleoids

Mitochondrial DNA (mtDNA) is organized in nucleoprotein particles called nucleoids. Each nucleoid, which is considered a heritable unit of mtDNA, might contain several copies of the mitochondrial genome and several different proteins. Some nucleoid-associated proteins, such as the high mobility group (HMG) box family, have well defined functions in mtDNA maintenance and packaging; others, such as Aco1 and IIv5, are bifunctional, fulfilling their roles in nucleoids in addition to well established metabolic functions. The fact that the HMG box mtDNA packaging proteins are of eukaryotic rather than bacterial origin and also that every organism seems to have a unique set of nucleoid-associated proteins suggests that evolutionary tinkering occurred to reinvent mitochondrial nucleoprotein during the evolution of mitochondrial genomes.     

Suitability of mitochondrial DNA for assaying interindividual genetic variation in small helminths.

The current paucity of data on the genetic structure of parasitic helminth populations results partly from the lack of a suitable molecular technique for assigning genotypes to small individuals. This report describes the cloning of the mitochondrial DNA (mtDNA) from a small parasitic nematode, Ostertagia ostertagi, and the potential use of this cloned mtDNA as a hybridization probe to detect genetic variation among individuals. By using cloned, homologous mtDNA, labeled to high specific activity, mtDNA restriction site variation can be assayed among individual O. ostertagi for at least 10 restriction enzymes.     

Evolutionary implications of analyses of complete mitochondrial genomes across order Zoantharia (Cnidaria: Hexacorallia)

Cnidarians are early-diverging metazoans, but evolutionary aspects of some taxa are still poorly understood, as in the order Zoantharia (Anthozoa: Hexacorallia). Zoantharians have been divided into two suborders based on the arrangement of the fifth septae as complete (Macrocnemina) or incomplete (Brachycnemina). Previous molecular phylogenetic analyses have indicated the need for re-evaluation as Macrocnemina has been found to be paraphyletic. Despite many phylogenetic studies, the recovery of complete mitochondrial genomes (mt-genomes) for systematic and evolutionary studies of zoantharians has been limited. The present study represents the first to sequence the complete mt-genomes of members of eight of nine zoantharian families. Although all examined mt-genomes had the same gene order arrangement, there were variations among mt-genomes' sizes, nucleotide substitution rates, and introns. Only two species did not have the cox1 intron, which harbors a gene coding a homing endonuclease of the LAGLIDADG type. Our mitogenomic analyses also showed relatively high nucleotide diversity in mt-DNA regions other than the standard regions traditionally considered for DNA barcoding of this group. Phylogenetic analyses using 13 mt-genome protein-coding genes recovered a fully resolved tree with clear separation between macrocnemic representatives. Ancestral state reconstruction analyses revealed three main transitions in arrangement of the marginal musculature through the evolutionary history of the order. An “early” transition from reticulate mesogleal to a cteniform endodermal arrangement was followed by transitions that occurred in the common ancestor of the Brachycnemina and family Hydrozoanthidae. Our results indicate the need for clarification of higher-level phylogeny and taxonomy of Zoantharia.     

The maintenance of mitochondrial genetic variation by negative frequency‐dependent selection

Mitochondrial genes generally show high levels of standing genetic variation, which is puzzling given the accumulating evidence for phenotypic effects of mitochondrial genetic variation. Negative frequency‐dependent selection, where the relative fitness of a genotype is inversely related to its frequency in a population, provides a potent and potentially general process that can maintain mitochondrial polymorphism. We assessed the change in mitochondrial haplotype frequencies over 10 generations of experimental evolution in 180 seed beetle populations in the laboratory, where haplotypes competed for propagation to subsequent generations. We found that haplotypes consistently increased in frequency when they were initially rare and decreased in frequency when initially common. Our results have important implications for the use of mtDNA haplotype frequency data to infer population level processes and they revive the general hypothesis that negative frequency‐dependent selection, presumably caused by habitat heterogeneity, may commonly promote polymorphism in ecologically relevant life history genes.     

Zoogeographical implications of variation in mitochondrial DNA of Arctic grayling (Thymallus arcticus)

Most of the northern half of North America's freshwater fish survived the last glacial period in unfrozen refugia peripheral to the ice sheets. In our study, the question of which refugia Arctic grayling ( Thymallus arcticus ) inhabited during the Wisconsinan Ice Age, and how they subsequently dispersed to their present geographical range, was examined using mitochondrial DNA (mtDNA) analysis. mtDNA from 12 T. arcticus populations was analysed by direct sequencing and restriction fragment length polymorphism analysis (RFLP). Our data support the hypotheses that T. arcticus had a large refugial population in the Bering Refuge (shown by high mtDNA diversity in extant Alaskan populations) and that British Columbia was colonized from the Bering Refuge (shown by mtDNA haplotype similarities). Our data also show that a disjunct southern set of populations in Montana is significantly different from the northern grayling, in terms of restriction haplotype frequency and distinguishing sequence characteristics. Sequence results yielded an estimated divergence time of 370 000 years between the northern and Montana grayling haplotypes. We conclude that T. arcticus survived the Wisconsinan glaciation in at least two refugia: (i) the Bering Refuge north of the ice sheets; and (ii) either the Upper Missouri or the southwest Alberta Refuge, south of the ice sheet.