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Dowling, D.

Publications and source records attributed to Dowling, D..

6 recordsLinked to original sources

Dissecting contributions of directional and balancing selection to trajectories of mitochondrial haplotype evolution in Drosophila melanogaster.

Emerging evidence suggests mtDNA haplotypes contribute to fitness variation and local adaptation, with studies highlighting the potential for directional selection, imposed by distinct thermal environments, and negative frequency-dependent selection to shape spatial patterns of mtDNA haplotype diversity. However, the interplay between these different forms of selection remains unexplored. To address this, we conducted experimental evolution using Drosophila melanogaster populations derived from opposite ends of a latitudinal cline in Australia (Melbourne and Townsville), exposing them to contrasting thermal environments and varying starting frequencies of two mtDNA haplotypes (A1 and B1) that each segregate at high frequencies in natural populations. We paired this approach with population genetic simulations to estimate selection and its influence on haplotype evolutionary trajectories. We found that mtDNA haplotype frequencies were influenced by complex interactions among temperature, starting frequency, and nuclear genomic background (Melbourne, Townsville, or admixed). Simulations supported directional selection as a driver of haplotype frequencies in populations evolving at 17{degrees}C in the Melbourne background, and otherwise selection was predominantly balancing and shaped by negative frequency-dependent fitness effects of the haplotypes. Finally, our results suggest that the thermal environment is not the sole environmental variable shaping mitochondrial evolutionary dynamics and point to a possible role for mito-nuclear epistasis.

evolutionary biology↗

Assessing the role of mitonuclear interactions on mitochondrial function and organismal fitness in natural Drosophila populations

Mitochondrial metabolism is regulated by a series of enzyme complexes, whose function depends on effective interactions between proteins and RNA encoded by the mitochondrial and nuclear genomes. These epistatic interactions are in turn highly sensitive to the environment. Many studies have found that mitochondrial haplotype frequencies of various taxa associate with latitude or altitude, leading to the hypothesis that mitochondrial genomes may respond to thermal selection and contribute to local adaptation. We used a Drosophila melanogaster panel comprising native (coadapted) populations from the extremes of the Australian east-coast cline, and generated mitonuclear cybrid populations. Our results indicate a strong phenotypic impact of mitonuclear interactions in cybrid lines, involving an apparent trade-off between aerobic capacity and key fitness aspects such as reproduction, growth, and survival. Overall, our study shows that naturally-occurring mitonuclear disruptions can have a meaningful impact on phenotypes, potentially influencing future ecological adaptation and population persistence.

evolutionary biology↗

Sex-specific transgenerational effects of diet on offspring life history and physiology

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 diets differing in sucrose concentration prior to reproduction, and similarly subjected grandoffspring to the same treatments. We then investigated the phenotypic consequences of this dietary variation among grandsons and granddaughters. We demonstrate 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.

evolutionary biology↗

Sexually antagonistic evolution of mitochondrial and nuclear linkage

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 it 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, while 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.

evolutionary biology↗

Individuality, as well as genotype, affects characteristics and temporal consistency of courtship songs in male mice

Courtship songs in mice have been investigated to understand the mechanisms and ecological relevance of vocal communication. There is evidence that courtship song characteristics vary between different genotypes, but little is known on whether individuals, even within the same genotype, differ from each other in the composition, complexity, and temporal consistency of their songs. In a first study, we aimed to systematically identify song features typical of different genotypes, by assessing the composition and complexity (i.e., entropy) of the syllabic sequences of male laboratory mice from four different strains (Mus musculus f. domestica: C57BL/6J, BALB/c, DBA/2 and B6D2F1). Mice were individually presented with a swab containing fresh female urine for 5 minutes to elicit courtship songs. The four strains differed not only in the composition but also in the complexity of their syllabic sequences. In a second study, we investigated within-strain individual differences in temporal consistency and recurring motifs (i.e., identical sets of syllables that are repeated within a song), using BALB/c and DBA/2 mice. The same procedure as in the first study was followed, but in addition testing was repeated weekly over three weeks. Both strains showed some level of individual temporal consistency; BALB/c in the overall amount of emitted vocalisations and DBA/2 in the expression of specific syllable types. However, hierarchical cluster analysis revealed remarkable individual variability in how consistent song characteristics were over time. Furthermore, recurring motifs were expressed at varying levels depending on the individual. Taken together, not only genotype but also individuality can affect variability in courtship songs in mice, suggesting the existence of different courtship strategies (e.g., higher song consistency to facilitate individual identification) related to varying levels of behavioural plasticity. HIGHLIGHTSO_LICourtship songs in mice can serve as a model to study vocal communication C_LIO_LIWe explore how genotype and individuality affect courtship songs characteristics C_LIO_LIGenotypes differ in composition and also in complexity of syllabic sequences C_LIO_LIWe find remarkable individual variability in how consistent songs are over time C_LIO_LIResults suggest the existence of variation in male courting behaviour C_LI

animal behavior and cognition↗

Mitochondrial genome variation affects the mutation rate of the nuclear genome in Drosophila melanogaster

Mutations are the raw material for evolutionary change. While the mutation rate has been thought constant between individuals, recent research has shown that poor genetic condition can elevate the mutation rate. Mitonuclear genetic conflict is a potential source of poor genetic condition, and considering the high mutation rate of mitochondrial genomes, there should be ample scope for mitochondrial mutations to interfere with genetic condition, with concomitant effects on the nuclear mutation rate. Moreover, because theory suggests mitochondrial genetic effects will often be male-biased, such effects could be more strongly felt in males than females. Here, by mating irradiated male Drosophila melanogaster to isogenic females bearing six distinct mitochondrial haplotypes, we tested whether mitochondrial genetic variation affects DNA repair capacity, and whether effects of mutation load on reproductive function are shaped by interactions between sex and mitochondrial haplotype. We found mitochondrial genetic effects on DNA repair, and that the mutational variance of reproductive fitness was higher in males bearing haplotypes characterized by high female fitness. These results suggest that mitochondrial genome variation may affect the mutation rate, and that induced mutations interact more strongly with male than female reproductive function. The potential for haplotype-specific effects on the nuclear mutation rate has broad implications for evolutionary dynamics, such as the accumulation of genetic load, adaptive potential, and the evolution of sexual dimorphism.

evolutionary biology↗