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Sexual selection has been suggested to influence the expression of male behavioral consistency. However, despite predictions, direct experimental support for this hypothesis has been lacking. Here, we investigated whether sexual selection altered male behavioral consistency in Drosophila melanogaster —a species with both pre- and postcopulatory sexual selection. We took 1,144 measures of locomotor activity (a fitness-related trait in D. melanogaster) from 286 flies derived from replicated populations that have experimentally evolved under either high or low levels of sexual selection for >320 generations. We found that high sexual selection males were more consistent (decreased within-individual variance) in their locomotor activity than male conspecifics from low sexual selection populations. There were no differences in behavioral consistency between females from the high and low sexual selection populations. Furthermore, while females were more behaviorally consistent than males in the low sexual selection populations, there were no sex differences in behavioral consistency in high sexual selection populations. Our results demonstrate that behavioral plasticity is reduced in males from populations exposed to high levels of sexual selection. Disentangling whether these effects represent an evolved response to changes in the intensity of selection or are manifested through nongenetic parental effects represents a challenge for future research. [ABSTRACT FROM AUTHOR]

Dietary variation in males and females can shape the expression of offspring life histories and physiology. However, the relative contributions of maternal and paternal dietary variation to phenotypic expression of latter generations is currently unknown. We provided male and female Drosophila melanogaster grandparents with diets differing in sucrose concentration prior to reproduction, and similarly subjected their grandoffspring to the same treatments. We then investigated the phenotypic consequences of this dietary variation among the grandsons and granddaughters. We observed transgenerational effects of dietary sucrose, mediated through the grandmaternal lineage, which mimic the direct effects of sucrose on lifespan, with opposing patterns across sexes; low sucrose increased female, but decreased male, lifespan. Dietary mismatching of grandoffspring–grandparent diets increased lifespan and reproductive success, and moderated triglyceride levels of grandoffspring, providing insights into the physiological underpinnings of the complex transgenerational effects on life histories. [ABSTRACT FROM AUTHOR]

Nutrition is a primary determinant of health, but responses to nutrition vary with genotype. Epistasis between mitochondrial and nuclear genomes may cause some of this variation, but which mitochondrial loci and nutrients participate in complex gene-by-gene-by-diet interactions? Furthermore, it remains unknown whether mitonuclear epistasis is involved only in the immediate responses to changes in diet, or whether mitonuclear genotype might modulate sensitivity to variation in parental nutrition, to shape intergenerational fitness responses. Here, in Drosophila melanogaster, we show that mitonuclear epistasis shapes fitness responses to variation in dietary lipids and amino acids. We also show that mitonuclear genotype modulates the parental effect of dietary lipid and amino acid variation on offspring fitness. Effect sizes for the interactions between diet, mitogenotype, and nucleogenotype were equal to or greater than the main effect of diet for some traits, suggesting that dietary impacts cannot be understood without first accounting for these interactions. Associating phenotype to mtDNA variation in a subset of populations implicated a C/T polymorphism in mt:lrRNA, which encodes the 16S rRNA of the mitochondrial ribosome. This association suggests that directionally different responses to dietary changes can result from variants on mtDNA that do not change protein coding sequence, dependent on epistatic interactions with variation in the nuclear genome. Why do genetically distinct individuals show differing responses to dietary change? This study investigates how genetic differences in mitochondria and the nucleus interact to determine fitness response to direct manipulation of diet, finding that the effects depend on essential amino acids and lipids, and a SNP in the mitochondrial 16S rRNA. [ABSTRACT FROM AUTHOR]

Mitochondria are key to energy conversion in virtually all eukaryotes. Intriguingly, despite billions of years of evolution inside the eukaryote, mitochondria have retained their own small set of genes involved in the regulation of oxidative phosphorylation (OXPHOS) and protein translation. Although there was a long-standing assumption that the genetic variation found within the mitochondria would be selectively neutral, research over the past 3 decades has challenged this assumption. This research has provided novel insight into the genetic and evolutionary forces that shape mitochondrial evolution and broader implications for evolutionary ecological processes. Many of the seminal studies in this field, from the inception of the research field to current studies, have been conducted using Drosophila flies, thus establishing the species as a model system for studies in mitochondrial evolutionary biology. In this review, we comprehensively review these studies, from those focusing on genetic processes shaping evolution within the mitochondrial genome, to those examining the evolutionary implications of interactions between genes spanning mitochondrial and nuclear genomes, and to those investigating the dynamics of mitochondrial heteroplasmy. We synthesize the contribution of these studies to shaping our understanding of the evolutionary and ecological implications of mitochondrial genetic variation. [ABSTRACT FROM AUTHOR]

While mitochondria have long been understood to be critical to cellular function, questions remain as to how genetic variation within mitochondria may underlie variation in general metrics of organismal function. To date, studies investigating links between mitochondrial genotype and phenotype have largely focused on differences in expression of genes and physiological and life‐history traits across haplotypes. Mating display behaviours may also be sensitive to mitochondrial functionality and so may also be affected by sequence variation in mitochondrial DNA, with consequences for sexual selection and fitness. Here, we tested whether the pre‐copulatory mating success of male fruit flies (Drosophila melanogaster) varies across six different mitochondrial haplotypes expressed alongside a common nuclear genetic background. We found a significant effect of mitochondrial haplotype on our measure of competitive mating success, driven largely by the relatively poor performance of males with one particular haplotype. This haplotype, termed 'Brownsville', has previously been shown to have complex and sex‐specific effects, most notably including depressed fertility in males but not females. Our study extends this disproportionate effect on male reproductive success to pre‐copulatory aspects of reproduction. Our results demonstrate that mutations in mitochondrial DNA can plausibly affect pre‐copulatory mating success, with implications for future study into the subcellular underpinnings of such behaviours and the information they may communicate. [ABSTRACT FROM AUTHOR]

The influence of temperature on cyto-nuclear effects on egg-to-adult development time in seed beetles is assessed. The findings show 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 might promote the maintenance of polymorphism in mitochondrial genes.

The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.

Social and aggressive behaviours often affect the fitness of multiple interacting individuals simultaneously. Here, we assessed dyadic interactions in a colour-polymorphic cichlid fish, the red devil, Amphilophus labiatus. We found that sub-adult red devil pairs of smaller body size interacted more, and were more aggressive towards each other, than pairs comprising larger individuals. Interactions did not significantly differ between colour morphs, i.e. between dark, gold and heterotypic pairs. Interestingly, within a broad range of parameters, an automated measure of time that the two fish spent in close proximity was an accurate proxy for their level of aggression, as measured by an observer from video recordings. These results show that, between sub-adult red devils, (aggressive) interactions significantly depend on body size, but not colour morph, of the interacting individuals. In addition, the results support the use of automated data-gathering approaches as an appropriate tool for studies of aggression. [ABSTRACT FROM AUTHOR]

Intergenerational effects on offspring phenotypes occur in response to variation in both maternal and paternal nutrition. Because the combined maternal and paternal effects are rarely considered together, however, their relative contributions, and the capacity for interactions between parental diets to shape offspring life history and physiology are not understood.To address this, we altered the sucrose levels of adult fruit flies (Drosophila melanogaster) prior to mating, across two generations, producing parent–parent and parent–offspring combinations that were either matched or mismatched in dietary sucrose. We then measured life span, fecundity, body mass and triglyceride levels in parents and offspring.We reveal complex, non‐cumulative interactions, which involve diets of each parent and offspring, shape offspring phenotypes, but the effects were generally not consistent with an adaptive response to parental diet.Notably, we find that interacting parental flies (sires and dams) lived longer when their sucrose treatments were matched, but they produced shorter lived offspring.These results are suggestive of intergenerational conflict over optimal diets, and call for further research into the capacity, and mechanisms, for mismatches in parental environments to enhance offspring phenotype generally.Our study also indicates that studies of maternal and paternal effects will need embrace experimental designs with power to test for interactions between maternal and paternal environments if they are to fully understand the ecological and evolutionary significance of parental effects on offspring fitness. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]

Mitochondrial sequence variants affect phenotypic function, often through interaction with the nuclear genome. These "mitonuclear" interactions have been linked both to evolutionary processes and human health. The study of these interactions has focused on mechanisms regulating communication between mitochondrial and nuclear proteins; the role of mitochondrial (mt) RNAs has received little attention. Here, we show that small mt-RNAs bind to the nuclear protein Argonaute 2, and that nuclear miRNAs bind to mt-mRNAs. We identify one small mt-RNA that binds to Argonaute 2 in human tissues whose expression and sequence remain unchanged across vertebrates. Although analyses of CLEAR-CLIP sequencing data sets of human and mouse did not reveal consistent interactions between small mt-RNAs and nuclear mRNAs, we found that MT- ND4 and MT- ATP6 mRNAs are bound by different nuclear miRNAs in humans and mice. Our work homes in on previously unknown interactions between nuclear and small mt-RNAs, which may play key roles in intergenomic communication. [ABSTRACT FROM AUTHOR]

Uniparental inheritance (UPI) of mitochondria predominates over biparental inheritance (BPI) in most eukaryotes. However, examples of BPI of mitochondria, or paternal leakage, are becoming increasingly prevalent. Most reported cases of BPI occur in hybrids of distantly related sub-populations. It is thought that BPI in these cases is maladaptive; caused by a failure of female or zygotic autophagymachinery to recognize divergentmale-mitochondrial DNA 'tags'. Yet recent theory has put forward examples in which BPI can evolve under adaptive selection, and empirical studies across numerous metazoan taxa have demonstrated outbreeding depression in hybrids attributable to disruption of population-specificmitochondrial and nuclear genotypes (mitonuclear mismatch). Based on these developments, we hypothesize that BPI may be favoured by selection in hybridizing populations when fitness is shaped by mitonuclear interactions. We test this idea using a deterministic, simulationbased population genetic model and demonstrate that BPI is favoured over strict UPI under moderate levels of gene flow typical of hybridizing populations. Our model suggests that BPI may be stable, rather than a transient phenomenon, in hybridizing populations. [ABSTRACT FROM AUTHOR]

Much research has focused on the effects of pathogenic mitochondrial mutations on health. Notwithstanding, the mechanisms regulating the link between these mutations and their effects remain elusive in several cases. Here, we propose that certain mitochondrial mutations may disrupt function of a set of mitochondrial‐transcribed small RNAs, perturbing communication between mitochondria and nucleus, leading to disease. Our hypothesis synthesises two lines of supporting evidence. First, several mitochondrial mutations cannot be directly linked to effects on energy production or protein synthesis. Second, emerging studies have described the existence of small RNAs encoded by the mitochondria and proposed their involvement in RNA interference. We present a roadmap to testing this hypothesis. [ABSTRACT FROM AUTHOR]

Abstract Background Biologists studying adaptation under sexual selection have spent considerable effort assessing the relative importance of two groups of models, which hinge on the idea that females gain indirect benefits via mate discrimination. These are the good genes and genetic compatibility models. Quantitative genetic studies have advanced our understanding of these models by enabling assessment of whether the genetic architectures underlying focal phenotypes are congruent with either model. In this context, good genes models require underlying additive genetic variance, while compatibility models require non-additive variance. Currently, we know very little about how the expression of genotypes comprised of distinct parental haplotypes, or how levels and types of genetic variance underlying key phenotypes, change across environments. Such knowledge is important, however, because genotype-environment interactions can have major implications on the potential for evolutionary responses to selection. Results We used a full diallel breeding design to screen for complex genotype-environment interactions, and genetic architectures underlying key morphological traits, across two thermal environments (the lab standard 27°C, and the cooler 23°C) in the Australian field cricket, Teleogryllus oceanicus. In males, complex three-way interactions between sire and dam parental haplotypes and the rearing environment accounted for up to 23 per cent of the scaled phenotypic variance in the traits we measured (body mass, pronotum width and testes mass), and each trait harboured significant additive genetic variance in the standard temperature (27°C) only. In females, these three-way interactions were less important, with interactions between the paternal haplotype and rearing environment accounting for about ten per cent of the phenotypic variance (in body mass, pronotum width and ovary mass). Of the female traits measured, only ovary mass for crickets reared at the cooler temperature (23°C), exhibited significant levels of additive genetic variance. Conclusions Our results show that the genetics underlying phenotypic expression can be complex, context-dependent and different in each of the sexes. We discuss the implications of these results, particularly in terms of the evolutionary processes that hinge on good and compatible genes models.

Across eukaryotes, genes encoding bioenergetic machinery are located in both mitochondrial and nuclear DNA, and incompatibilities between the two genomes can be devastating. Mitochondria are often inherited maternally, and theory predicts sex‐specific fitness effects of mitochondrial mutational diversity. Yet how evolution acts on linkage patterns between mitochondrial and nuclear genomes is poorly understood. Using novel mito‐nuclear population‐genetic models, we show that the interplay between nuclear and mitochondrial genes maintains mitochondrial haplotype diversity within populations, and selects both for sex‐independent segregation of mitochondrion‐interacting genes and for paternal leakage. These effects of genetic linkage evolution can eliminate male‐harming fitness effects of mtDNA mutational diversity. With maternal mitochondrial inheritance, females maintain a tight mitochondrial–nuclear match, but males accumulate mismatch mutations because of the weak statistical associations between the two genomic components. Sex‐independent segregation of mitochondria‐interacting loci improves the mito‐nuclear match. In a sexually antagonistic evolutionary process, male nuclear alleles evolve to increase the rate of recombination, whereas females evolve to suppress it. Paternal leakage of mitochondria can evolve as an alternative mechanism to improve the mito‐nuclear linkage. Our modelling framework provides an evolutionary explanation for the observed paucity of mitochondrion‐interacting genes on mammalian sex chromosomes and for paternal leakage in protists, plants, fungi and some animals. [ABSTRACT FROM AUTHOR]

Genetic variation outside of the cell nucleus can affect the phenotype. The cytoplasm is home to the mitochondria, and in arthropods often hosts intracellular bacteria such as Wolbachia. Although numerous studies have implicated epistatic interactions between cytoplasmic and nuclear genetic variation as mediators of phenotypic expression, two questions remain. Firstly, it remains unclear whether outcomes of cyto‐nuclear interactions will manifest differently across the sexes, as might be predicted given that cytoplasmic genomes are screened by natural selection only through females as a consequence of their maternal inheritance. Secondly, the relative contribution of mitochondrial genetic variation to other cytoplasmic sources of variation, such as Wolbachia infection, in shaping phenotypic outcomes of cyto‐nuclear interactions remains unknown. Here, we address these questions, creating a fully crossed set of replicated cyto‐nuclear populations derived from three geographically distinct populations of Drosophila melanogaster, measuring the lifespan of males and females from each population. We observed that cyto‐nuclear interactions shape lifespan and that the outcomes of these interactions differ across the sexes. Yet, we found no evidence that placing the cytoplasms from one population alongside the nuclear background of others (generating putative cyto‐nuclear mismatches) leads to decreased lifespan in either sex. Although it was difficult to partition mitochondrial from Wolbachia effects, our results suggest at least some of the cytoplasmic genotypic contribution to lifespan was directly mediated by an effect of sequence variation in the mtDNA. Future work should explore the degree to which cyto‐nuclear interactions result in sex differences in the expression of other components of organismal life history. [ABSTRACT FROM AUTHOR]

Many traits correlate with body size. Studies that seek to uncover the ecological factors that drive evolutionary responses in traits typically examine these responses relative to associated changes in body size using multiple regression analysis. However, it is not well appreciated that in the presence of strongly correlated variables, the partial (i.e., relative) regression coefficients often change sign compared to the original coefficients. Such sign reversals are difficult to interpret in a biologically meaningful way, and could lead to erroneous evolutionary inferences if the true mechanism underlying the sign reversal differed from the proposed mechanism. Here, we use simulations to demonstrate that sign reversal occurs over a wide range of parameter values common in the biological sciences. Further, as a case‐in‐point, we review the literature on brain size evolution; a field that explores how ecological traits relate to the evolution of relative brain size (brain size relative to body size). We find that most studies show sign reversals and thus that the inferences of many studies in this field may be inconclusive. Finally, we propose some approaches to mitigating this issue. [ABSTRACT FROM AUTHOR]

Maternal inheritance of mitochondrial DNA (mtDNA) was originally thought to prevent any response to selection on male phenotypic variation attributable to mtDNA, resulting in a male‐biased mtDNA mutation load ("mother's curse"). However, the theory underpinning this claim implicitly assumes that a male's mtDNA has no effect on the fitness of females he comes into contact with. If such "mitochondrially encoded indirect genetics effects" (mtIGEs) do in fact exist, and there is relatedness between the mitochondrial genomes of interacting males and females, male mtDNA‐encoded traits can undergo adaptation after all. We tested this possibility using strains of Drosophila melanogaster that differ in their mtDNA. Our experiments indicate that female fitness is influenced by the mtDNA carried by males that the females encounter, which could plausibly allow the mitochondrial genome to evolve via kin selection. We argue that mtIGEs are probably common, and that this might ameliorate or exacerbate mother's curse. [ABSTRACT FROM AUTHOR]

A random selection of 25 mitochondrial founders from a single, panmictic population of Drosophila melanogaster is tested to see whether there is within-population variation in cytoplasmic genes for female longevity and senescence. Significant cytoplasmic effects of longevity, Gompertz intercept (frailty) and demographic rate of change in morality with age was reported in females providing evidence that genetic variation in cytoplasmic genes contributes to variation in female mortality and aging.

Maternal inheritance of mitochondrial DNA (mtDNA) renders selection blind to mutations whose effects are limited to males. Evolutionary theory predicts this will lead to the accumulation of a male-specific genetic load within the mitochondrial genomes of populations; that is, a pool of mutations that negatively affects male, but not female, fitness components. This principle has been termed the Mother's Curse hypothesis. While the hypothesis has received some empirical support, its relevance to natural populations of metazoans remains unclear, and these ambiguities are compounded by the lack of a clear predictive framework for studies attempting to test Mother's Curse. Here, we seek to redress this by outlining the core predictions of the hypothesis, as well as the key features of the experimental designs that are required to enable direct testing of the predictions. Our goal is to provide a roadmap for future research seeking to elucidate the evolutionary significance of the Mother's Curse hypothesis. [ABSTRACT FROM AUTHOR]

Substantial evidence suggests that individuals born to overweight and obese parents suffer detrimental health consequences that dramatically decrease healthy aging. The number of obese individuals worldwide now exceeds the number of under- and malnourished individuals. This obesity epidemic is responsible for approximately 4 million deaths worldwide each year, and predisposes sufferers to a range of age-related diseases such as cardiovascular diseases, and metabolic syndrome. Additionally, obesity is associated with an accelerated onset of age-related ailments, such as cancers and inflammation. The importance of dietary interventions to reduce the incidence of obesity is magnified by emerging evidence that parental physiology can predispose future generations to poor health outcomes. Characterizing and understanding these effects, and how they are mediated, is important if we are to continue to drive improvements to population health. In this article, we synthesize evidence for the intergenerational and transgenerational phenotypic effects of parental obesity. We concentrate on how the fruit fly Drosophila melanogaster can be used as a model to study these effects. Fruit flies are highly tractable, and their conserved nutrient signaling and metabolic pathways make them an ideal model for studying nutritional effects on metabolic, reproductive, and aging phenotypes. [ABSTRACT FROM AUTHOR]

Eukaryotes are the outcome of an ancient symbiosis and as such, eukaryotic cells fundamentally possess two genomes. As a consequence, gene products encoded by both nuclear and mitochondrial genomes must interact in an intimate and precise fashion to enable aerobic respiration in eukaryotes. This genomic architecture of eukaryotes is proposed to necessitate perpetual coevolution between the nuclear and mitochondrial genomes to maintain coadaptation, but the presence of two genomes also creates the opportunity for intracellular conflict. In the collection of papers that constitute this symposium volume, scientists working in diverse organismal systems spanning vast biological scales address emerging topics in integrative, comparative biology in light of mitonuclear interactions. [ABSTRACT FROM AUTHOR]

Recent studies have demonstrated that modifications to the ratio of dietary macronutrients affect longevity in a diverse range of species. However, the degree to which levels of natural genotypic variation shape these dietary effects on longevity remains unclear. The mitochondria have long been linked to the aging process. The mitochondria possess their own genome, and previous studies have shown that mitochondrial genetic variation affects longevity in insects. Furthermore, the mitochondria are the sites in which dietary nutrients are oxidized to produce adenosine triphosphate, suggesting a capacity for dietary quality to mediate the link between mitochondrial genotype and longevity. Here, we measured longevity of male and female fruit flies, across a panel of genetic strains of Drosophila melanogaster, which vary only in their mitochondrial haplotype, when fed one of the two isocaloric diets that differed in their protein-to-carbohydrate ratio. The mitochondrial haplotype affected the longevity of flies, but the pattern of these effects differed across the two diets in males, but not in females. We discuss the implications of these results in relation to an evolutionary theory linking maternal inheritance of mitochondria to the accumulation of male-harming mitochondrial mutations, and to the theory exploring the evolution of phenotypic plasticity to novel environments. [ABSTRACT FROM AUTHOR]

Several studies have linked mitochondrial genetic variation to phenotypic modifications; albeit the identity of the mitochondrial polymorphisms involved remains elusive. The search for these polymorphisms led to the discovery of small noncoding RNAs, which appear to be transcribed by the mitochondrial DNA ("small mitochondrial RNAs"). This contention is, however, controversial because the nuclear genome of most animals harbors mitochondrial pseudogenes (NUMTs) of identical sequence to regions of mtDNA, which could alternatively represent the source of these RNAs. To discern the likely contributions of the mitochondrial and nuclear genome to transcribing these small mitochondrial RNAs, we leverage data from six vertebrate species exhibiting markedly different levels of NUMT sequence. We explore whether abundances of small mitochondrial RNAs are associated with levels of NUMT sequence across species, or differences in tissue-specific mtDNA content within species. Evidence for the former would support the hypothesis these RNAs are primarily transcribed by NUMT sequence, whereas evidence for the latter would provide strong evidence for the counter hypothesis that these RNAs are transcribed directly by the mtDNA. No association exists between the abundance of small mitochondrial RNAs and NUMT levels across species. Moreover, a sizable proportion of transcripts map exclusively to the mtDNA sequence, even in species with highest NUMT levels. Conversely, tissue-specific abundances of small mitochondrial RNAs are strongly associated with the mtDNA content. These results support the hypothesis that small mitochondrial RNAs are primarily transcribed by the mitochondrial genome and that this capacity is conserved across Amniota and, most likely, across most metazoan lineages. [ABSTRACT FROM AUTHOR]