Temperature-specific outcomes of cytoplasmic-nuclear interactions on egg-to-adult development time in seed beetles

The integration of the mitochondrial and nuclear genomes coordinates cellular energy production and is fundamental to life among eukaryotes. Therefore, there is potential for strong selection to shape the interactions between the two genomes. Several studies have now demonstrated that epistatic interactions between cytoplasmic and nuclear genes for fitness can occur both at a "within" and "across" population level. Genotype-by-environment interactions are common for traits that are encoded by nuclear genes, but the effects of environmental heterogeneity on traits that are partly encoded by cytoplasmic genes have received little attention despite the fact that there are reasons to believe that phenotypic effects of cytoplasmic genetic variation may often be environment specific. Consequently, the importance of environmental heterogeneity to the outcomes of cyto-nuclear fitness interactions and to the maintenance of mitochondrial polymorphism is unclear. Here, we assess the influence of temperature on cyto-nuclear effects on egg-to-adult development time in seed beetles (Callosobruchus maculatus). We employed an "across-population" design, sourcing beetles from five distinct populations and using backcrossing to create orthogonal combinations of distinct introgression lines, fixed for their cytoplasmic and nuclear lineages. We then assayed development times at two different temperatures and found sizeable cyto-nuclear effects in general, as well as temperature- and block-specific cyto-nuclear effects. These results demonstrate that environmental factors such as temperature do exert selection on cytoplasmic genes by favoring specific cyto-nuclear genetic combinations, and are consistent with the suggestion that complex genotype-by-environment interactions may promote the maintenance of polymorphism in mitochondrial genes.     

A meta‐analysis of the strength and nature of cytoplasmic genetic effects

Genetic variation in cytoplasmic genomes (i.e. the mitochondrial genome in animals, and the combined mitochondrial and chloroplast genomes in plants) was traditionally assumed to accumulate under a neutral equilibrium model. This view has, however, come under increasing challenge from studies that have experimentally linked cytoplasmic genetic effects to the expression of life history phenotypes. Such results suggest that genetic variance located within the cytoplasm might be of evolutionary importance and potentially involved in shaping population evolutionary trajectories. As a step towards assessing this assertion, here we conduct a formal meta‐analytic review to quantitatively assess the extent to which cytoplasmic genetic effects contribute to phenotypic expression across animal and plant kingdoms. We report that cytoplasmic effect sizes are generally moderate in size and associated with variation across a range of factors. Specifically, cytoplasmic effects on morphological traits are generally larger than those on life history or metabolic traits. Cytoplasmic effect sizes estimated at the between‐species scale (via interspecies mix‐and‐matching of cytoplasmic and nuclear genomes) are larger than those at the within‐species scale. Furthermore, cytoplasmic effects tied to epistatic interactions with the nuclear genome tend to be stronger than additive cytoplasmic effects, at least when restricting the data set to gonochorous animal species. Our results thus confirm that cytoplasmic genetic variation is commonly tied to phenotypic expression across plants and animals, implicate the cytoplasmic–nuclear interaction as a key unit on which natural selection acts and generally suggest that the genetic variation that lies within the cytoplasm is likely to be entwined in adaptive evolutionary processes.     

A theoretical model for quantitatively inherited traits influenced by nuclear-cytoplasmic interactions

Summary Cytoplasmic genes of crop species exhibit non-Mendelian inheritance and affect quantitative traits such as biomass and grain yield. Photosynthesis and respiration are physiological processes responsible, in part, for the expression of such quantitative traits and are regulated by enzymes encoded in both the cytoplasm and nucleus. Cytoplasmic genes are located in the chloroplast and mitochondrial genomes. Unlike the nuclear genome, the cytoplasmic genomes consist of single, circular, double-stranded molecules of DNA, and in many crop species, the cytoplasmic genomes are inherited solely through the maternal parent. Maternal inheritance of cytoplasmic genomes and Mendelian inheritance of the nuclear genome were used to model the genotypic value of an individual. The model then was utilized to derive genetic variances and covariances for a random-mating population. Finally, the use of reciprocal mating designs to estimate variance components was investigated.Journal Paper No. J-12457 of the Iowa Agric. and Home Econ. Exp. Stn., Ames, IA 50011. Project No. 2447     

Outbreeding selects for spiteful cytoplasmic elements

In addition to their nuclear genome, the vast majority of eukaryotes harbour cytoplasmic genomes, e.g. in mitochondria or chloroplasts. In the majority of cases, these cytoplasmic genomes are transmitted maternally only, leading to selective pressures divergent from those that act on nuclear genes. In particular, cytoplasmic genes, which reduce the fitness of males that carry them, but have no fitness effect in females, are believed to be selectively neutral. Here, we go a step further and argue that in outbreeding populations (i.e. populations with inbreeding avoidance), 'spiteful' cytoplasmic elements that reduce the number of offspring produced by males are in fact selected for. We study this process by means of a stochastic model, analysing both the probability of spread and the impact that such a spiteful cytotype can have on population dynamics. Our results demonstrate that the probability of spread of the spiteful cytotype can be several times higher in outbreeding than in panmictic populations. Spread and fixation of the spiteful cytotype can lead to different qualitative effects on the population dynamics, including extinction, decreased or increased stable population size. We discuss our results in respect to cytoplasmically induced male infertility and cytoplasmic incompatibility.     

The on‐again,off‐again relationship between mitochondrial genomes and species boundaries

The study of reproductive isolation and species barriers frequently focuses on mitochondrial genomes and has produced two alternative and almost diametrically opposed narratives. On one hand, mtDNA may be at the forefront of speciation events, with co‐evolved mitonuclear interactions responsible for some of the earliest genetic incompatibilities arising among isolated populations. On the other hand, there are numerous cases of introgression of mtDNA across species boundaries even when nuclear gene flow is restricted. We argue that these seemingly contradictory patterns can result from a single underlying cause. Specifically, the accumulation of deleterious mutations in mtDNA creates a problem with two alternative evolutionary solutions. In some cases, compensatory or epistatic changes in the nuclear genome may ameliorate the effects of mitochondrial mutations, thereby establishing coadapted mitonuclear genotypes within populations and forming the basis of reproductive incompatibilities between populations. Alternatively, populations with high mitochondrial mutation loads may be rescued by replacement with a more fit, foreign mitochondrial haplotype. Coupled with many nonadaptive mechanisms of introgression that can preferentially affect cytoplasmic genomes, this form of adaptive introgression may contribute to the widespread discordance between mitochondrial and nuclear genealogies. Here, we review recent advances related to mitochondrial introgression and mitonuclear incompatibilities, including the potential for cointrogression of mtDNA and interacting nuclear genes. We also address an emerging controversy over the classic assumption that selection on mitochondrial genomes is inefficient and discuss the mechanisms that lead lineages down alternative evolutionary paths in response to mitochondrial mutation accumulation.     

CYTONUCLEAR INTERACTIONS CAN FAVOR THE EVOLUTION OF GENOMIC IMPRINTING

Interactions between cytoplasmic (generally organelle) and nuclear genomes may be relatively common and could potentially have major fitness consequences. As in the case of within-genome epistasis, this cytonuclear epistasis can favor the evolutionary coadaptation of high-fitness combinations of nuclear and cytoplasmic alleles. Because cytoplasmic factors are generally uniparentally inherited, the cytoplasmic genome is inherited along with only one of the nuclear haplotypes, and therefore, coadaptation is expected to evolve through the interaction of these coinherited (usually maternally inherited) genomes. Here I show that, as a result of this coinheritance of the two genomes, cytonuclear epistasis can favor the evolution of genomic imprinting such that, when the cytoplasmic factor is maternally inherited, selection favors maternal expression of the nuclear locus and when the factor is paternally inherited selection favors paternal expression. Genomic imprinting evolves in this model because it leads to a pattern of gene expression in the nuclear haplotype that is coadapted with (i.e., adaptively coordinated with) gene expression in the coinherited cytoplasmic genome.     

Sex-Limited Mitochondrial DNA Transmission in the Marine Mussel Mytilus Edulis

Mitochondrial DNA (mtDNA) was thought to be inherited maternally in animals, although paternal leakage has been reported in mice and Drosophila. Recently, direct evidence of extensive paternal inheritance of mtDNA has been found in the marine mussel Mytilus. We give evidence that whereas female mussels are homoplasmic for a genome that is transmitted to eggs, male mussels are heteroplasmic for this genome and for a second genome that is transmitted preferentially to sperm. The results provide support for the existence of separate male and female routes of mtDNA inheritance in mussels. The two genomes show a base sequence divergence exceeding 20% at three protein coding genes, consistent with long term maintenance of the heteroplasmic state. We propose that the two genomes differ in fitness in males and females, possibly as a result of interaction with nuclear genes.     

The conversion of variance and the evolutionary potential of restricted recombination

Genetic recombination is usually considered to facilitate adaptive evolution. However, recombination prevents the reliable cotransmission of interacting gene combinations and can disrupt complexes of coadapted genes. If interactions between genes have important fitness effects, restricted recombination may lead to evolutionary responses that are different from those predicted from a purely additive model and could even aid adaptation. Theory and data have demonstrated that phenomena that limit the effectiveness of recombination via increasing homozygosity, such as inbreeding and population subdivision and bottlenecks, can temporarily increase the additive genetic variance available to these populations. This effect has been attributed to the conversion of nonadditive to additive genetic variance. Analogously, phenomena such as chromosomal inversions and apomictic parthenogenesis that physically restrict recombination in part or all of the genome may also result in a release of additive variance. Here, we review and synthesize literature concerning the evolutionary potential of populations with effectively or physically restricted recombination. Our goal is to emphasize the common theme of increased short-term access to additive genetic variance in all of these situations and to motivate research directed towards a more complete characterization of the relevance of the conversion of variance to the evolutionary process.     

A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle

It is widely assumed that male sperm competitiveness evolves adaptively. However, recent studies have found a cytoplasmic genetic component to phenotypic variation in some sperm traits presumed important in sperm competition. As cytoplasmic genes are maternally transmitted, they cannot respond to selection on sperm and this constraint may affect the scope in which sperm competitiveness can evolve adaptively. We examined nuclear and cytoplasmic genetic contributions to sperm competitiveness, using populations of Callosobruchus maculatus carrying orthogonal combinations of nuclear and cytoplasmic lineages. Our design also enabled us to examine genetic contributions to female remating. We found that sperm competitiveness and remating are primarily encoded by nuclear genes. In particular, a male's sperm competitiveness phenotype was contingent on an interaction between the competing male genotypes. Furthermore, cytoplasmic effects were detected on remating but not sperm competitiveness, suggesting that cytoplasmic genes do not generally play a profound evolutionary role in sperm competition.     

Intergenomic interactions between mitochondrial and Y‐linked genes shape male mating patterns and fertility in Drosophila melanogaster

Under maternal inheritance, mitochondrial genomes are prone to accumulate mutations that exhibit male‐biased effects. Such mutations should, however, place selection on the nuclear genome for modifier adaptations that mitigate mitochondrial‐incurred male harm. One gene region that might harbor such modifiers is the Y‐chromosome, given the abundance of Y‐linked variation for male fertility, and because Y‐linked modifiers would not exert antagonistic effects in females because they would be found only in males. Recent studies in Drosophila revealed a set of nuclear genes whose expression is sensitive to allelic variation among mtDNA‐ and Y‐haplotypes, suggesting these genes might be entwined in evolutionary conflict between mtDNA and Y. Here, we test whether genetic variation across mtDNA and Y haplotypes, sourced from three disjunct populations, interacts to affect male mating patterns and fertility across 10 days of early life in D. melanogaster. We also investigate whether coevolved mito‐Y combinations outperform their evolutionarily novel counterparts, as predicted if the interacting Y‐linked variance is comprised of modifier adaptations. Although we found no evidence that coevolved mito‐Y combinations outperformed their novel counterparts, interactions between mtDNA and Y‐chromosomes affected male mating patterns. These interactions were dependent on male age; thus male reproductive success was shaped by G × G × E interactions.     

Adaptive co‐evolution of mitochondria and the Y‐chromosome: A resolution to conflict between evolutionary opponents

In most species with motile sperm, male fertility depends upon genes located on the Y‐chromosome and in the mitochondrial genome. Coordinated adaptive evolution for the function of male fertility between genes on the Y and the mitochondrion is hampered by their uniparental inheritance in opposing sexes: The Y‐chromosome is inherited uniparentally, father to son, and the mitochondrion is inherited maternally, mother to offspring. Preserving male fertility is problematic, because maternal inheritance permits mitochondrial mutations advantageous to females, but deleterious to male fertility, to accumulate in a population. Although uniparental inheritance with sex‐restricted adaptation also affects genes on the Y‐chromosome, females lack a Y‐chromosome and escape the potential maladaptive consequences of male‐limited selection. Evolutionary models have shown that mitochondrial mutations deleterious to male fertility can be countered by compensatory evolution of Y‐linked mutations that restore it. However, direct adaptive coevolution of Y‐ and mitochondrial gene combinations has not yet been mathematically characterized. We use population genetic models to show that adaptive coevolution of Y and mitochondrial genes are possible when Y‐mt gene combinations have positive effects on male fertility and populations are inbred.     

Concordant evolution of mitochondrial and nuclear genomes in the wheat pathogen Phaeosphaeria nodorum

We compared patterns of mitochondrial restriction fragment length polymorphism (RFLP) diversity with patterns of nuclear RFLP diversity to investigate the effects of selection, gene flow, and sexual reproduction on the population genetic structure and evolutionary history of the wheat pathogen Phaeosphaeria nodorum. A total of 315 fungal isolates from Texas, Oregon, and Switzerland were analyzed using seven nuclear RFLP probes that hybridized to discrete loci and purified mitochondrial DNA that hybridized to the entire mtDNA genome. Forty-two different mitochondrial haplotypes and 298 different nuclear haplotypes were detected. The two most frequent mtDNA haplotypes were present in every population and represented 32% of all isolates. High levels of gene flow, low levels of population subdivision, no evidence for either host specificity or cyto-nuclear disequilibrium were inferred from the analysis of both genomes. The concordance in estimates of these population genetic parameters from both genomes suggests that the two genomes experienced similar degrees of migration, genetic drift and selection.     

THE EFFECT OF NUCLEAR AND CYTOPLASMIC GENES ON FITNESS AND LOCAL ADAPTATION IN AN ANNUAL LEGUME,CHAMAECRISTA FASCICULATA

The role of nuclear genes in local adaptation has been well documented. However, the role of maternally inherited cytoplasmic genes to the evolution of natural populations has been relatively unstudied. To evaluate the contribution of cytoplasmic and nuclear genomes and their interactions to local adaptation we created second-generation backcross hybrids between a Maryland and an Illinois population of the annual legume Chamaecrista fasciculata. Backcross progeny were planted in the sites native to each population for two years and we quantified germination, survivorship, fruit production, vegetative biomass, and cumulative fitness. We found limited evidence for the contribution of either cytoplasmic or nuclear genes to local adaptation. In Maryland plants had greater survivorship, biomass, fruit production, and cumulative fitness if their nuclear genome was composed predominately of native Maryland genes; cytoplasmic genes did not affect fitness. In Illinois local cytoplasm marginally enhanced fitness, whereas Maryland nuclear genes outperformed local nuclear genes. Interactions between cytoplasmic and nuclear genes influenced seed weight, vegetative biomass, and fitness and therefore may affect evolution of these characters. Genetic effects were stronger acting through seed size than directly on characters. However, seed size differences between the two populations were largely genetic and therefore selection on fitness components is likely to result in evolutionary change. The contribution of nuclear and cytoplasmic genes to fitness components varied across sites and years, suggesting that experiments should be replicated and conducted under natural conditions to understand the influence of these genomes and their interactions to population differentiation.     

Patterns of cyto-nuclear linkage disequilibrium in Silene latifolia: genomic heterogeneity and temporal stability

Non-random association of alleles in the nucleus and cytoplasmic organelles, or cyto-nuclear linkage disequilibrium (LD), is both an important component of a number of evolutionary processes and a statistical indicator of others. The evolutionary significance of cyto-nuclear LD will depend on both its magnitude and how stable those associations are through time. Here, we use a longitudinal population genetic data set to explore the magnitude and temporal dynamics of cyto-nuclear disequilibria through time. We genotyped 135 and 170 individuals from 16 and 17 patches of the plant species Silene latifolia in Southwestern VA, sampled in 1993 and 2008, respectively. Individuals were genotyped at 14 highly polymorphic microsatellite markers and a single-nucleotide polymorphism (SNP) in the mitochondrial gene, atp1. Normalized LD (D′) between nuclear and cytoplasmic loci varied considerably depending on which nuclear locus was considered (ranging from 0.005–0.632). Four of the 14 cyto-nuclear associations showed a statistically significant shift over approximately seven generations. However, the overall magnitude of this disequilibrium was largely stable over time. The observed origin and stability of cyto-nuclear LD is most likely caused by the slow admixture between anciently diverged lineages within the species'' newly invaded range, and the local spatial structure and metapopulation dynamics that are known to structure genetic variation in this system.     

Natural Selection with Nuclear and Cytoplasmic Transmission. II. Tests with Drosophila from Diverse Populations

Observations of intraspecific variation in organelle DNA have prompted a renewed interest in the evolutionary consequences of cytoplasmically transmitted factors. Attempts to quantify the significance of cytoplasmic effects are frequently limited by the difficulty in partitioning the cause of reciprocal cross differences among a series of possibilities. In the experiment reported here the nuclear genomes of a set of six lines of Drosophila melanogaster from diverse geographic locations were replaced in a series of cytoplasms. The segregation of the SM5 balancer chromosome was scored in a factorial design, and the data allowed a partitioning of variance such that cytoplasmic effects were distinguished from maternal effects and meiotic drive. An attempt was made to avoid the confounding problem of hybrid dysgenesis by performing the entire experiment (including chromosomal extractions) in a P cytotype. Results indicated a significant contribution of cytoplasm to the variance in SM5 segregation. Error variance showed an increasing trend as the experiment proceeded, and additional tests indicated that this was due to an accumulation of chromosomal mutations. These findings are interpreted in light of the population genetic theory that addresses the maintenance of cytoplasmic polymorphism.     

Inheritance through the cytoplasm

Most heritable information in eukaryotic cells is encoded in the nuclear genome, with inheritance patterns following classic Mendelian segregation. Genomes residing in the cytoplasm, however, prove to be a peculiar exception to this rule. Cytoplasmic genetic elements are generally maternally inherited, although there are several exceptions where these are paternally, biparentally or doubly-uniparentally inherited. In this review, we examine the diversity and peculiarities of cytoplasmically inherited genomes, and the broad evolutionary consequences that non-Mendelian inheritance brings. We first explore the origins of vertical transmission and uniparental inheritance, before detailing the vast diversity of cytoplasmic inheritance systems across Eukaryota. We then describe the evolution of genomic organisation across lineages, how this process has been shaped by interactions with the nuclear genome and population genetics dynamics. Finally, we discuss how both nuclear and cytoplasmic genomes have evolved to co-inhabit the same host cell via one of the longest symbiotic processes, and all the opportunities for intergenomic conflict that arise due to divergence in inheritance patterns. In sum, we cannot understand the evolution of eukaryotes without understanding hereditary symbiosis.Subject terms: Evolutionary genetics, Genetic variation     

基因组叠加生物型的基因表达特征

采用聚丙烯酰胺梯度凝胶电泳及特异性组织化学染色技术分析了鲤、鲫及其基因组叠加的不同组合个体的红细胞ＳＯＤ、ＥＳＴ和血红蛋白的电泳图谱。结果表明不同基因组合及不同倍性的个体间存在由基因组差异导致的生化多态性,为不同倍性的鱼类的同工酶（ＳＯＤ）表达存在基因剂量效应提供了依据,证实了不同组合的ＳＯＤ亚基间有协同表达、累积作用。研究表明每个基因有其独特的调控机制,因而在杂种三倍体内三分之一的基因组亦能够表     

The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited

Cytoplasmic male sterility (CMS) in plants is a classical example of genomic conflict, opposing maternally-inherited cytoplasmic genes (mitochondrial genes in most cases), which induce male sterility, and nuclear genes, which restore male fertility. In natural populations, this type of sex control leads to gynodioecy, that is, the co-occurrence of female and hermaphroditic individuals within a population. According to theoretical models, two conditions may maintain male sterility in a natural population: (1) female advantage (female plants are reproductively more successful than hermaphrodites on account of their global seed production); (2) the counter-selection of nuclear fertility restorers when the corresponding male-sterility-inducing cytoplasm is lacking. In this review, we re-examine the model of nuclear-mitochondrial conflict in the light of recent experimental results from naturally occurring CMS, alloplasmic CMS (appearing after interspecific crosses resulting from the association of nuclear and cytoplasmic genomes from different species), and CMS plants obtained in the laboratory and carrying mitochondrial mutations. We raise new hypotheses and discuss experimental models that would take physiological interactions between cytoplasmic and nuclear genomes into account.