Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis

Evolutionary theory proposes that maternal inheritance of mitochondria will facilitate the accumulation of mitochondrial DNA (mtDNA) mutations that are harmful to males but benign or beneficial to females. Furthermore, mtDNA haplotypes sampled from across a given species distribution are expected to differ in the number and identity of these ‘male-harming’ mutations they accumulate. Consequently, it is predicted that the genetic variation which delineates distinct mtDNA haplotypes of a given species should confer larger phenotypic effects on males than females (reflecting mtDNA mutations that are male-harming, but female-benign), or sexually antagonistic effects (reflecting mutations that are male-harming, but female-benefitting). These predictions have received support from recent work examining mitochondrial haplotypic effects on adult life-history traits in Drosophila melanogaster. Here, we explore whether similar signatures of male-bias or sexual antagonism extend to a key physiological trait—metabolic rate. We measured the effects of mitochondrial haplotypes on the amount of carbon dioxide produced by individual flies, controlling for mass and activity, across 13 strains of D. melanogaster that differed only in their mtDNA haplotype. The effects of mtDNA haplotype on metabolic rate were larger in males than females. Furthermore, we observed a negative intersexual correlation across the haplotypes for metabolic rate. Finally, we uncovered a male-specific negative correlation, across haplotypes, between metabolic rate and longevity. These results are consistent with the hypothesis that maternal mitochondrial inheritance has led to the accumulation of a sex-specific genetic load within the mitochondrial genome, which affects metabolic rate and that may have consequences for the evolution of sex differences in life history

Antidepressant exposure causes a nonmonotonic reduction in anxiety-related behaviour in female mosquitofish

Worldwide, biologically active pharmaceuticals, such as psychoactive drugs, are routinely detected in aquatic ecosystems. In this regard, selective serotonin reuptake inhibitors (SSRIs), a class of antidepressant, are of major environmental concern. Through targeted action on evolutionarily conserved physiological pathways, SSRIs could alter ecologically important behaviours in exposed organisms. Here, using two field-realistic dosages (measured concentrations: 18 and 215 ng/L) of the SSRI fluoxetine (Prozac), we examined the effects of exposure on anxiety-related behaviours in wild-caught female mosquitofish, Gambusia holbrooki. Anxiety-related behaviour was assessed using a light/dark transition test, with the swimming activity of fish recorded under two alternating light conditions, complete darkness and bright light, with the shift in light condition used to induce an anxiety-like response. Fluoxetine exposure resulted in a nonmonotonic decrease in anxiety-related behaviour (i.e. nonlinear with dose), with fish in the low-fluoxetine treatment being less responsive to shifts in light condition compared to unexposed fish. There was no such difference between unexposed and high-exposed fish. Further, we detected a significant interaction between exposure treatment and fish weight on general swimming activity, suggesting the presence of a mass-specific effect of fluoxetine. More broadly, contaminant-induced disruption of animal behaviour—as documented here—could have wide-reaching effects on population-level fitness

Diet and mitonuclear haplotype interactions affect growth rate in a slime mould

Abstract Trait expression in metazoans is strongly influenced by the balance of macronutrients (i.e. protein, carbohydrate and fat) in the diet. At the same time, an individual's genetic background seems to regulate the magnitude of phenotypic response to a particular diet. It needs to be better understood whether interactions between diet, genetic background and trait expression are found in unicellular eukaryotes. A protist—the slime mould, Physarum polycephalum can choose diets based on protein‐to‐carbohydrate (P:C) content to support optimal growth rate. Yet, the role of genetic background (variation in the mitochondrial and nuclear DNAs) in mediating growth rate response to dietary P:C ratios in the slime mould is unknown. Here, we studied the effects of interactions between mitochondrial and nuclear DNA haplotypes and diet (i.e. G × G × E interactions) on the growth rate of P. polycephalum. A genetic panel of six distinct strains of P. polycephalum that differ in their mitochondrial and nuclear DNA haplotypes was used to measure growth rate across five diets that varied in their P:C ratio and total calories. We first determined the strains' growth rate (total biomass and surface area) when grown on a set menu with access to a particular diet. We then assessed whether the growth rate of strains increased on a buffet menu with access to all diets. Our findings show that the growth rate of P. polycephalum is generally higher on diets containing more carbohydrates than protein and that total calories negatively affect the growth rate. Three‐way interactions between mitochondrial, nuclear haplotypes and dietary P:C ratios affected the strains' surface area of growth but not biomass. Intriguingly, strains did not increase their surface area and biomass when they had access to all diets on the buffet menu. Our findings have broad implications for our understanding of the effect of mitonuclear interactions on trait expression across diverse eukaryotic lineages

G×G×E effect on phenotype expression in the unicellular slime mould Physarum polycephalum

We developed a genetic panel of the unicellular slime mould, Physarum polycephalum containing strains differing in mitochondrial and nuclear DNA haplotypes. The panel included two strains harbouring a selfishly replicating mitochondrial-fusion (mF) plasmid that could affect phenotype expression. We assayed movement and growth rate differences among the strains across two temperature regimes: 24° and 28°C. The dataset contains raw data from growth rate and movement assays.</p

Interactions between mitochondrial haplotype and dietary macronutrient ratios confer sex-specific effects on longevity in Drosophila melanogaster

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 ageing 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 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

Field-realistic antidepressant exposure disrupts group foraging dynamics in mosquitofish

Psychoactive pollutants, such as antidepressants, are increasingly detected in the environment. Mounting evidence suggests that such pollutants can disrupt the behaviour of non-target species. Despite this, few studies have considered how the response of exposed organisms might be mediated by social context. To redress this, we investigated impacts of two environmentally realistic concentrations of a pervasive antidepressant pollutant, fluoxetine, on foraging behaviour in fish (Gambusia holbrooki), tested individually or in a group. Fluoxetine did not alter behaviour of solitary fish. However, in a group setting, fluoxetine exposure disrupted the frequency of aggressive interactions and food consumption, with observed effects being contingent on both the mean weight of group members and the level of within-group variation in weight. Our results suggest that behavioural tests in social isolation may not accurately predict the environmental risk of chemical pollutants for group-living species, and highlight the potential for social context to mediate the effects of psychoactive pollutants in exposed wildlife.Martin 2019 Biology letters forage morphThe morphological data for all fish used in the experiment.Martin 2019 Biology letters forage groupExperimental data from group foraging trials. Where fish have been exposed to one of three conditions, a freshwater control, low-fluoxetine (nominal: 30 ng/L), or high-fluoxetine (nominal: 300 ng/L).Martin 2019 Biology letters forage singleExperimental data from indivudal foraging trials. Where fish have been exposed to one of three conditions, a freshwater control, low-fluoxetine (nominal: 30 ng/L), or high-fluoxetine (nominal: 300 ng/L)

Size, more than colour, drives dyadic interactions in sub-adults of a colour polymorphic cichlid

Abstract 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