Publications


BMC Evolutionary Biology, August 2016

M Nystrand, EJ Cassidy, DK Dowling

Evolution, September 2015

Winston K.W. Yee, Bjorn Rogell, Bernardo Lemos and Damian K. Dowling

Current Biology, October 2015

M. Florencia Camus, Jochen B.W. Wolf, Edward H. Morrow, Damian K. Dowling

Journal of Evolutionary Biology, August 2015

Rebecca Dean, Bernardo Lemos, Damian K Dowling

BioEssays, July 2015

Justin C Havird, Matthew D Hall, Damian K Dowling

EMBO reports, May 2015

Edward H Morrow, Klaus Reinhardt, Jonci N Wolff, Damian K Dowling

Current Biology, October 2014

DK Dowling

Proceedings of the Royal Society B: Biological Sciences, October 2014

M Nystrand, DK Dowling

Journal of Evolutionary Biology, September 2014

R Dobler, B Rogell, F Budar, DK Dowling

Phil. Trans. R. Soc. B, May 2014

Jonci N. Wolff, Emmanuel D. Ladoukakis, José A. Enríquez and Damian K. Dowling

Phil. Trans. R. Soc. B, May 2014

Madeleine Beekman, Damian K. Dowling and Duur K. Aanen

BMC Genomics, May 2014

Björn Rogell, Rebecca Dean, Bernardo Lemos and Damian K Dowling

Journal of evolutionary biology, January 2014

DK Dowling, BR Williams, F Garcia‐Gonzalez

Biology letters, December 2013

Daniel Paz Decanini, Bob BM Wong, Damian K Dowling

Science, September 2013

Klaus Reinhardt, Damian K Dowling, Edward H Morrow

Current Biology, January 2013

WKW Yee, KL Sutton, DK Dowling

Current Biology, November 2012

DK Dowling

Current Biology, September 2012

MF Camus, DJ Clancy, DK Dowling

Journal of Evolutionary Biology, May 2012

BR Williams, B VAN Heerwaarden, DK Dowling, CM Sgrò

Ecology Letters, September 2011

M Almbro, DK Dowling, LW Simmons

Evolution, November 2010

G Arnqvist, DK Dowling, P Eady, L Gay, T Tregenza, M Tuda, DJ Hosken

The American Naturalist, June 2010

DK Dowling, T Meerupati, G Arnqvist

Proceedings of the Royal Society B: Biological Sciences, May 2009

DK Dowling, LW Simmons

Journal of Evolutionary Biology, April 2009

DK Dowling, AA Maklakov, U Friberg, F Hailer

Trends in Ecology & Evolution, October 2008

DK Dowling, U Friberg, J Lindell

Journal of Evolutionary Biology, November 2007

DK Dowling, U Friberg, G Arnqvist

Annales Zoologici Fennici, August 2006

DK Dowling, RA Mulder

Journal of Evolutionary Biology, March 2006

DK Dowling, RA Mulder

Behavioral Ecology, April 2005

NE Langmore, RM Kilner, SHM Butchart, G Maurer, NB Davies, A Cockburn, NA Macgregor, A Peters, MJL Magrath, DK Dowling

Australian Journal of Zoology, February 2004

DK Dowling

Petroica goodenovii. Emu, October 2003

DK Dowling, M Antos, T Sahlman

Journal of Avian Biology, December 2001

DK Dowling, DS Richardson, K Blaakmeer, J Komdeur

Scientific Reports, February 2017

M Nystrand, EJ Cassidy, DK Dowling

Mitochondrial genetic variation shapes the expression of life-history traits associated with reproduction, development and survival, and has also been associated with the prevalence and progression of infectious bacteria and viruses in humans. The breadth of these effects on multifaceted components of health, and their link to disease susceptibility, led us to test whether variation across mitochondrial haplotypes affected reproductive success following an immune challenge in the form of a non-infectious pathogen. We test this, by challenging male and female fruit flies (Drosophila melanogaster), harbouring each of three distinct mitochondrial haplotypes in an otherwise standardized genetic background, to either a mix of heat-killed bacteria, or a procedural control, prior to measuring their subsequent reproductive performance. The effect of the pathogen challenge on reproductive success did not differ across mitochondrial haplotypes; thus there was no evidence that patterns of reproductive plasticity were modified by the mitochondrial genotype following a non-infectious pathogen exposure. We discuss the implications of our data, and suggest future research avenues based on these results.

bioRxiv, Janurary 2017

Cellular metabolism is regulated by enzyme complexes within the mitochondrion, the function of which are sensitive to the prevailing temperature. Such thermal sensitivity, coupled with the observation that population frequencies of mitochondrial haplotypes tend to associate with latitude, altitude or climatic regions across species distributions, led to the hypothesis that thermal selection has played a role in shaping standing variation in the mitochondrial DNA (mtDNA) sequence. This hypothesis, however, remains controversial, and requires evidence the distribution of haplotypes observed in nature corresponds with the 30 capacity of these haplotypes to confer differences in thermal tolerance. Specifically, haplotypes predominating in tropical climates are predicted to encode increased tolerance to heat stress, but decreased tolerance to cold stress, than temperate counterparts. We present direct evidence for these predictions, using mtDNA haplotypes sampled from the Australian distribution of Drosophila melanogaster. We show that the ability of flies to tolerate extreme thermal challenges is affected by sequence variation across mtDNA haplotypes, and that the thermal performance associated with each haplotype corresponds with its latitudinal prevalence. The haplotype that predominates at low (subtropical) latitudes confers greater resilience to heat stress, but lower resilience to cold stress, than counterparts predominating at higher (temperate) latitudes. We explore molecular mechanisms that might underlie these responses, presenting evidence that the effects are in part regulated by SNPs that do not change the protein sequence. Our findings indicate that standing genetic variation in the mitochondrial genome can be shaped by thermal selection, and could therefore contribute to evolutionary adaptation under climatic stress.

Heredity, October 2016

AT Branco, L Schilling, K Silkaitis, DK Dowling, B Lemos

Reproduction and aging evolved to be intimately associated. Experimental selection for early-life reproduction drives the evolution of decreased longevity in Drosophila whereas experimental selection for increased longevity leads to changes in reproduction. Although life history theory offers hypotheses to explain these relationships, the genetic architecture and molecular mechanisms underlying reproduction–longevity associations remain a matter of debate. Here we show that mating triggers accelerated mortality in males and identify hundreds of genes that are modulated upon mating in the fruit fly Drosophila melanogaster. Interrogation of genome-wide gene expression in virgin and recently mated males revealed coherent responses, with biological processes that are upregulated (testis-specific gene expression) or downregulated (metabolism and mitochondria-related functions) upon mating. Furthermore, using a panel of genotypes from the Drosophila Synthetic Population Resource (DSPR) as a source of naturally occurring genetic perturbation, we uncover abundant variation in longevity and reproduction-induced mortality among genotypes. Genotypes displayed more than fourfold variation in longevity and reproduction-induced mortality that can be traced to variation in specific segments of the genome. The data reveal individual variation in sensitivity to reproduction and physiological processes that are enhanced and suppressed upon mating. These results raise the prospect that variation in longevity and age-related traits could be traced to processes that coordinate germline and somatic function.

BMC Evolutionary Biology, August 2016

M Nystrand, EJ Cassidy, DK Dowling

Phenotypic plasticity operates across generations, when the parental environment affects phenotypic expression in the offspring. Recent studies in invertebrates have reported transgenerational plasticity in phenotypic responses of offspring when the mothers had been previously exposed to either live or heat-killed pathogens. Understanding whether this plasticity is adaptive requires a factorial design in which both mothers and their offspring are subjected to either the pathogen challenge or a control, in experimentally matched and mismatched combinations. Most prior studies exploring the capacity for pathogen-mediated transgenerational plasticity have, however, failed to adopt such a design. Furthermore, it is currently poorly understood whether the magnitude or direction of pathogen-mediated transgenerational responses will be sensitive to environmental heterogeneity. Here, we explored the transgenerational consequences of a dual pathogen and stress challenge administered in the maternal generation in the fruit fly, Drosophila melanogaster. Prospective mothers were assigned to a non-infectious pathogen treatment consisting of an injection with heat-killed bacteria or a procedural control, and a stress treatment consisting of sleep deprivation or control. Their daughters and sons were similarly assigned to the same pathogen treatment, prior to measurement of their reproductive success.

Scientific Reports, January 2016

JN Wolff, DM Tompkins, NJ Gemmell, DK Dowling

Pest species pose major challenges to global economies, ecosystems, and health. Unfortunately, most conventional approaches to pest control remain costly, and temporary in effect. As such, a heritable variant of the Sterile Insect Technique (SIT) was proposed, based on the introduction of mitochondrial DNA mutations into pest populations, which impair male fertility but have no effects on females. Evidence for this “Trojan Female Technique” (TFT) was recently provided, in the form of a mutation in the mitochondrial cytochrome b gene (mt:Cyt-b) of Drosophila melanogaster which reduces male fertility across diverse nuclear backgrounds. However, recent studies have shown that the magnitude of mitochondrial genetic effects on the phenotype can vary greatly across environments, with mtDNA polymorphisms commonly entwined in genotype-by-environment (G × E) interactions. Here we test whether the male-sterilizing effects previously associated with the mt:Cyt-b mutation are consistent across three thermal and three nuclear genomic contexts. The effects of this mutation were indeed moderated by the nuclear background and thermal environment, but crucially the fertility of males carrying the mutation was invariably reduced relative to controls. This mutation thus constitutes a promising candidate for the further development of the TFT.

Journal of Evolutionary Biology, January 2016

JN Wolff, N Pichaud, MF Camus, G Côté, PU Blier, DK Dowling

The ancient acquisition of the mitochondrion into the ancestor of modernday 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.

Evolution, December 2015

Jonci N. Wolff, M. Florencia Camus, David J. Clancy, and Damian K. Dowling

The complete mitogenomes of 13 strains of the fruit fly Drosophila melanogaster were sequenced. Haplotypes varied between 19 532 and 19 537 bp in length, and followed standard dipteran mitogenome content and organization. We detected a total of 354 variable sites between all thirteen haplotypes, while single pairs of haplotypes were separated by an average of 123 variable sites. The sequenced fly strains form a powerful model for mitochondrial research, when it comes to elucidating the links between the mitochondrial genotype and the phenotype.

Evolution, September 2015

Winston K.W. Yee, Bjorn Rogell, Bernardo Lemos and Damian K. Dowling

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.

Current Biology, October 2015

M. Florencia Camus, Jochen B.W. Wolf, Edward H. Morrow, Damian K. Dowling

Camus et al. report that small changes to the mtDNA sequence affect mitochondrial gene expression and mtDNA copy number. They then map single-base-pair changes in mtDNA to the expression of mitochondrial proteincoding genes and show that these effects have sex-specific—even sexually antagonistic—consequences on fertility and longevity.

Evolutionary Applications, October 2015

Damian K Dowling, Daniel M Tompkins, Neil J Gemmell

Pest species represent a major ongoing threat to global biodiversity. Effective management approaches are required that regulate pest numbers, while minimising collateral damage to non-target species. The Trojan Female Technique (TFT) was recently proposed as a
prospective approach to biological pest control. The TFT draws on the evolutionary hypothesis that maternally-inherited mitochondrial genomes are prone to the accumulation of male, but not female, harming mutations. These mutations could be harnessed to provide trans-generational fertility-based control of pest species. A candidate TFT mutation was recently described in the fruit fly, Drosophila melanogaster, which confers male-only sterility in the specific isogenic nuclear background in which it is maintained. However, applicability of the TFT relies on mitochondrial mutations whose male-sterilizing effects are general across nuclear genomic contexts. We test this assumption, expressing the candidate TFT-mutation bearing haplotype alongside a range of nuclear backgrounds and comparing its fertility in males, relative to that of control haplotypes. We document consistently lower fertility for males harbouring the TFT mutation, in both competitive and non-competitive mating contexts, across all nuclear backgrounds screened. This indicates that TFT mutations conferring reduced male fertility can segregate within populations, and could be harnessed to facilitate this novel form of pest control.

Journal of Evolutionary Biology, August 2015

Rebecca Dean, Bernardo Lemos, Damian K Dowling

Some regions of the genome exhibit sexual asymmetries in inheritance and are thus subjected to sex-biased evolutionary forces. Maternal inheritance of mitochondrial DNA (mtDNA) enables mtDNA mutations harmful to males, but not females, to accumulate. In the face of male-harmful mtDNA mutation accumulation, selection will favour the evolution of compensatory modifiers in the nuclear genome that offset fitness losses to males. The Y chromosome is a candidate to host these modifiers, because it is paternally inherited, known to harbour an abundance of genetic variation for male fertility, and therefore likely to be under strong selection to uphold male viability. Here, we test for intergenomic interactions involving mtDNA and Y chromosomes in male Drosophila melanogaster. Specifically, we examine effects of each of these genomic regions, and their interaction, on locomotive activity, across different environmental contexts – both dietary and social. We found that both the mtDNA haplotype and Y chromosome haplotype affected activity in males assayed in an environment perceived as social. These effects, however, were not evident in males assayed in perceived solitary environments, and neither social nor solitary treatments revealed evidence for intergenomic interactions. Finally, the magnitude and direction of these genetic effects was further contingent on the diet treatment of the males. Thus, genes within the mtDNA and Y chromosome are involved in genotype-by-environment interactions. These interactions might contribute to the maintenance of genetic variation within these asymmetrically inherited gene regions and complicate the dynamics of genetic interactions between the mtDNA and the Y chromosome.

BioEssays, July 2015

Justin C Havird, Matthew D Hall, Damian K Dowling

The evolution of sex in eukaryotes represents a paradox, given the twofold fitness cost it incurs. We hypothesize that the mutational dynamics of the mitochondrial genome would have favored the evolution of sexual reproduction. Mitochondrial DNA (mtDNA) exhibits a high-mutation rate across most eukaryote taxa, and several lines of evidence suggest that this high rate is an ancestral character. This seems inexplicable given that mtDNA-encoded genes underlie the expression of life’s most salient functions, including energy conversion. We propose that negative metabolic effects linked to mitochondrial mutation accumulation would have invoked selection for sexual recombination between divergent host nuclear genomes in early eukaryote lineages. This would provide a mechanism by which recombinant host genotypes could be rapidly shuffled and screened for the presence of compensatory modifiers that offset mtDNA-induced harm. Under this hypothesis, recombination provides the genetic variation necessary for compensatory nuclear coadaptation to keep pace with mitochondrial mutation accumulation.

EMBO reports, May 2015

Edward H Morrow, Klaus Reinhardt, Jonci N Wolff, Damian K Dowling

The UK Parliament recently debated and then approved legislation to allow mitochondrial replacement (MR) to be used in the clinic. However, we are concerned that some of the science of MR has been misunderstood or otherwise given only fleeting consideration. We set out our arguments below and offer a way forward to ensure that MR can safely deliver the health benefits it promises for those suffering from mitochondrial-related diseases.

Biology letters, March 2015

Francisco Garcia-Gonzalez, Damian K Dowling

The consequences of sexual interactions extend beyond the simple production of offspring. These interactions typically entail direct effects on female fitness, but may also impact the life histories of later generations. Evaluating the cross-generational effects of sexual interactions provides insights into the dynamics of sexual selection and conflict. Such studies can elucidate whether offspring fitness optima diverge across sexes upon heightened levels of sexual interaction among parents. Here, we found that, in Drosophila melanogaster, components of reproductive success in females, but not males, were contingent on the nature of sexual interactions experienced by their mothers. In particular, maternal sexual interactions with non-sires enhanced female fecundity in the following generation. This highlights the importance of non-sire influences of sexual interactions on the expression of offspring life histories.

Current Biology, October 2014

DK Dowling

A new study reports that male, but not female, longevity evolves in response to increasing male mortality. The sex gap in longevity widens depending on the type of mortality.

Proceedings of the Royal Society B: Biological Sciences, October 2014

M Nystrand, DK Dowling

It is well established that the parental phenotype can influence offspring phenotypic expression, independent of the effects of the offspring's own genotype. Nonetheless, the evolutionary implications of such parental effects remain unclear, partly because previous studies have generally overlooked the potential for interactions between parental sources of non-genetic variance to influence patterns of offspring phenotypic expression. We tested for such interactions, subjecting male and female Drosophila melanogaster of two different age classes to an immune activation challenge or a control treatment. Flies were then crossed in all age and immune status combinations, and the reproductive success of their immune- and control-treated daughters measured. We found that daughters produced by two younger parents exhibited reduced reproductive success relative to those of other parental age combinations. Furthermore, immune-challenged daughters exhibited higher reproductive success when produced by immune-challenged relative to control-treated mothers, a pattern consistent with transgenerational immune priming. Finally, a complex interplay between paternal age and parental immune statuses influenced daughter's reproductive success. These findings demonstrate the dynamic nature of age- and immune-mediated parental effects, traceable to both parents, and regulated by interactions between parents and between parents and offspring.

Journal of Evolutionary Biology, September 2014

R Dobler, B Rogell, F Budar, DK Dowling

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.

Phil. Trans. R. Soc. B, May 2014

Jonci N. Wolff, Emmanuel D. Ladoukakis, José A. Enríquez and Damian K. Dowling

Fundamental biological processes hinge on coordinated interactions between genes spanning two obligate genomes—mitochondrial and nuclear. These interactions are key to complex life, and allelic variation that accumulates and persists at the loci embroiled in such intergenomic interactions should therefore be subjected to intense selection to maintain integrity of the mitochondrial electron transport system. Here, we compile evidence that suggests that mitochondrial–nuclear (mitonuclear) allelic interactions are evolutionarily significant modulators of the expression of key health-related and life-history phenotypes, across several biological scales—within species (intra- and interpopulational) and between species. We then introduce a new frontier for the study of mitonuclear interactions—those that occur within individuals, and are fuelled by the mtDNA heteroplasmy and the existence of nuclear-encoded mitochondrial gene duplicates and isoforms. Empirical evidence supports the idea of high-resolution tissue- and environment-specific modulation of intraindividual mitonuclear interactions. Predicting the penetrance, severity and expression patterns of mtDNA-induced mitochondrial diseases remains a conundrum. We contend that a deeper understanding of the dynamics and ramifications of mitonuclear interactions, across all biological levels, will provide key insights that tangibly advance our understanding, not only of core evolutionary processes, but also of the complex genetics underlying human mitochondrial disease.

Phil. Trans. R. Soc. B, May 2014

Madeleine Beekman, Damian K. Dowling and Duur K. Aanen

Eukaryotic cells typically contain numerous mitochondria, each with multiple copies of their own genome, the mtDNA. Uniparental transmission of mitochondria, usually via the mother, prevents the mixing of mtDNA from different individuals. While on the one hand, this should resolve the potential for selection for fast-replicating mtDNA variants that reduce organismal fitness, maternal inheritance will, in theory, come with another set of problems that are specifically relevant to males. Maternal inheritance implies that the mitochondrial genome is never transmitted through males, and thus selection can target only the mtDNA sequence when carried by females. A consequence is that mtDNA mutations that confer male-biased phenotypic expression will be prone to evade selection, and accumulate. Here, we review the evidence from the ecological, evolutionary and medical literature for male specificity of mtDNA mutations affecting fertility, health and ageing. While such effects have been discovered experimentally in the laboratory, their relevance to natural populations—including the human population—remains unclear. We suggest that the existence of male expression-biased mtDNA mutations is likely to be a broad phenomenon, but that these mutations remain cryptic owing to the presence of counter-adapted nuclear compensatory modifier mutations, which offset their deleterious effects.

BMC Genomics, May 2014

Björn Rogell, Rebecca Dean, Bernardo Lemos and Damian K Dowling

Mito-nuclear gene interactions regulate energy conversion, and are fundamental to eukaryotes. Generally, mito-nuclear coadaptation would be most efficient if the interacting nuclear genes were X-linked, because this maximizes the probability of favorable mito-nuclear allelic combinations co-transmitting across generations. Thus, under a coadaptation (CA) hypothesis, nuclear genes essential for mitochondrial function might be under selection to relocate to the X-chromosome. However, maternal inheritance predisposes the mitochondrial DNA (mtDNA) to accumulate variation that, while male-harming, is benign to females. Numerous nuclear genes were recently reported in Drosophila melanogaster, which exhibit male-specific patterns of differential expression when placed alongside different mtDNA haplotypes, suggesting that nuclear genes are sensitive to an underlying male-specific mitochondrial mutation load. These genes are thus candidates for involvement in mito-nuclear interactions driven by sexual conflict (SC), and selection might have moved them off the X-chromosome to facilitate an optimal evolutionary counter-response, through males, to the presence of male-harming mtDNA mutations. Furthermore, the presence of male-harming mtDNA mutations could exert selection for modifiers on the Y-chromosome, thus placing these mito-sensitive nuclear genes at the center of an evolutionary tug-of-war between mitochondrion and Y-chromosome.

Journal of Evolutionary Biology, April 2014

M Nystrand, DK Dowling

Immune responses are highly dynamic. The magnitude and efficiency of an immune response to a pathogen can change markedly across individuals, and such changes may be influenced by variance in a range of intrinsic (e.g. age, genotype, sex) and external (e.g. abiotic stress, pathogen identity, strain) factors. Life history theory predicts that up-regulation of the immune system will come at a physiological cost, and studies have confirmed that increased investment in immunity can reduce reproductive output and survival. Furthermore, males and females often have divergent reproductive strategies, and this might drive the evolution of sex-specific life history trade-offs involving immunity, and sexual dimorphism in immune responses per se. Here, we employ an experiment design to elucidate dose-dependent and sex-specific responses to exposure to a nonpathogenic immune elicitor at two scales – the ‘ultimate’ life history and the underlying ‘proximate’ immune level in Drosophila melanogaster. We found dose-dependent effects of immune challenges on both male and female components of reproductive success, but not on survival, as well as a response in antimicrobial activity. These results indicate that even in the absence of the direct pathogenic effects that are associated with actual disease, individual life histories respond to a perceived immune challenge – but with the magnitude of this response being contingent on the initial dose of exposure. Furthermore, the results indicate that immune responses at the ultimate life history level may indeed reflect underlying processes that occur at the proximate level.

Biochimica et Biophysica Acta, April 2014

Damian K Dowling

Background: Disorders of the mitochondrial respiratory chain are heterogeneous in their symptoms and under- lying genetics. Simple links between candidate mutations and expression of disease phenotype typically do not exist. It thus remains unclear how the genetic variation in the mitochondrial genome contributes to the phenotypic expression of complex traits and disease phenotypes. Scope of review: I summarize the basic genetic processes known to underpin mitochondrial disease. I highlight other plausible processes, drawn from the evolutionary biological literature, whose contribution to mitochondrial disease expression remains largely empirically unexplored. I highlight recent advances to the field, and discuss common-ground and -goals shared by researchers across medical and evolutionary domains. Major conclusions: Mitochondrial genetic variance is linked to phenotypic variance across a variety of traits (e.g. reproductive function, life expectancy) fundamental to the upkeep of good health. Evolutionary theory predicts that mitochondrial genomes are destined to accumulate male-harming (but female-friendly) mutations, and this prediction has received proof-of-principle support. Furthermore, mitochondrial effects on the phenotype are typically manifested via interactions between mitochondrial and nuclear genes. Thus, whether a mitochondrial mutation is a pathogenic in effect can depend on the nuclear genotype in which is it expressed. General significance: Many disease phenotypes associated with OXPHOS malfunction might be determined by the outcomes of mitochondrial–nuclear interactions, and by the evolutionary forces that historically shaped mitochondrial DNA (mtDNA) sequences. Concepts and results drawn from the evolutionary sciences can have broad, but currently under-utilized, applicability to the medical sciences and provide new insights into under- standing the complex genetics of mitochondrial disease. This article is part of a Special Issue entitled Frontiers of Mitochondrial Research.

Journal of evolutionary biology, January 2014

DK Dowling, BR Williams, F Garcia-Gonzalez

In many species, females exposed to increased sexual activity experience reductions in longevity. Here, in Drosophila melanogaster, we report an additional effect on females brought about by sexual interactions, an effect that spans generations. We subjected females to a sexual treatment consisting of different levels of sexual activity and then investigated patterns of mortality in their offspring. We found reduced probabilities of survival, increases in the rate of senescence and a pattern of reduced mean longevities, for offspring produced by mothers that experienced higher levels of sexual interaction. We contend that these effects constitute trans-generational costs of sexual conflict – the existence or implications of which have rarely been considered previously. Our results indicate that ongoing exposure by mothers to male precopulatory interactions is itself sufficient to drive transgenerational effects on offspring mortality. Thus, we show that increases in maternal sexual activity can produce trans-generational effects that permeate through to latter life stages in the offspring. This helps to elucidate the complex interplay between sex and ageing and provides new insights into the dynamics of adaptation under sexual selection.

Biology letters, December 2013

Daniel Paz Decanini, Bob BM Wong, Damian K Dowling

In most species, females mate multiply within a reproductive cycle, invoking post-copulatory selection on ejaculatory components. Much research has focused on disentangling the key traits important in deciding the outcomes of sperm competition and investigating patterns of covariance among these traits. Less attention has focused on the degree to which such patterns might be context-dependent. Here,we examine whether the expression of sperm viability— a widely used measure of sperm quality—and patterns of covariance between this trait and male reproductive morphologies, change across distinct age classes and across naturally occurring genotypes, when expressed in both heterozygotic (extreme outbred) and homozygotic (extreme inbred) states in the fruitfly Drosophila melanogaster. Older males, and heterozygous males, generally exhibited higher sperm viability. The male age effect seems at least partly explained by a positive association between sperm numbers and viability. First, old males possessed more stored sperm than young males, and second, sperm numbers and viability were also positively associated within each age class. Furthermore, we found a positive association between sperm viability and testis size, but only among heterozygous, old males. These results suggest that sperm quality is a labile trait, with expression levels that are context-dependent and shaped by multiple, potentially interacting, factors.

Science, September 2013

Klaus Reinhardt, Damian K Dowling, Edward H Morrow

Health outcomes of intraspecies experimental MR in animals. Studies either invasively removed the nucleus by placing it into the enucleated donor oocyte (blue shading) or replaced mitochondria by repeatedly crossing foreign mitochondrial genotypes into nuclear backgrounds (green shading)(see table S1 for details). All species share the same 37 mitochondrial encoded genes. Studies of health effects of MR on vertebrates that have reached reproductive ages are lacking.

Current Biology, January 2013

WKW Yee, KL Sutton, DK Dowling

We harness an experimental design that enables us to completely disentangle mitochondrial from nuclear genetic effects in the fruit fly Drosophila melanogaster. Using this design, we directly link male fertility outcomes to the mitochondrial haplotype. Specifically, we show that competitive male fertility, measured in vivo, differs across naturally occurring mitochondrial haplotypes. We discuss this result in the context of recent studies that support the evolutionary hypothesis according to which maternal inheritance of mitochondria will facilitate the accumulation of male-harming mutations in the mitochondrial genome, when these same mutations are benign, beneficial or slightly deleterious in their effects on females [1–3]. We predict that at least some of the mitochondrial allelic variance affecting competitive male fertility across the sampled haplotypes will have accumulated under this evolutionary process and be male specific in its effect on the phenotype. We suggest that the existence of male-harming mitochondrial mutations for male fertility would place strong selection on the interacting nuclear genome to evolve compensatory counter-adaptations that offset the negative effects, and we present support for this idea.

Current Biology, November 2012

DK Dowling

Most people seem to realize that death is an inevitable consequence of life. For those individuals that don’t suffer a premature death at the hands of extrinsic hazards of mortality, such as predation (Figure 1), infectious disease or accidents, a slower physiological deterioration invariably awaits. It is this deterioration that is aging — the intrinsic component of mortality —and it has captured widespread interest among evolutionary biologists for well over a century [1]. A new study by Chen and Maklakov in this issue of Current Biology [2] has shown that in nematodes life span evolves when populations experience increases in the rate of extrinsic mortality. Remarkably, the direction of this evolutionary response hinges on the type of mortality. These findings help to explain why empirical tests of classic theories of aging have hitherto provided an inconclusive set of results.

Current Biology, September 2012

MF Camus, DJ Clancy, DK Dowling

The maternal transmission of mitochondrial genomes invokes a sex-specific selective sieve, whereby mutations in mitochondrial DNA can only respond to selection acting directly on females [1–3]. In theory, this enables male-harming mutations to accumulate in mitochondrial genomes when these same mutations are neutral, beneficial, or only slightly deleterious in their effects on females [1–3]. Ultimately, this evolutionary process could result in the evolution of male-specific mitochondrial mutation loads; an idea previously termed Mother’s Curse [2, 4–6]. Here, we present evidence that the effects of this process are broader than hitherto realized, and that it has resulted in mutation loads affecting patterns of aging in male, but not female Drosophila melanogaster. Furthermore, our results indicate that the mitochondrial mutation loads affecting male aging generally comprise numerous mutations over multiple sites. Our findings thus suggest that males are subject to dramatic consequences that result from the maternal transmission of mitochondrial genomes. They implicate the diminutive mitochondrial genome as a hotspot for mutations that affect sex-specific patterns of aging, thus promoting the idea that a sex-specific selective sieve in mitochondrial genome evolution is a contributing factor to sexual dimorphism in aging, commonly observed across species [7–9].

Journal of Evolutionary Biology, May 2012

BR Williams, B VAN Heerwaarden, DK Dowling, CM Sgrò

Exposure to extreme temperatures is increasingly likely to impose strong selection on many organisms in their natural environments. The ability of organisms to adapt to such selective pressures will be determined by patterns of genetic variation and covariation. Despite increasing interest in thermal adaptation, few studies have examined the extent to which the genetic covariance between traits might constrain thermal responses. Furthermore, it remains unknown whether sex-specific genetic architectures will constrain responses to climatic selection. We used a paternal half-sibling breeding design to examine whether sex-specific genetic architectures and genetic covariances between traits might constrain evolutionary responses to warming climates in a population of Drosophila melanogaster. Our results suggest that the sexes share a common genetic underpinning for heat tolerance as indicated by a strong positive inter-sexual genetic correlation. Further, we found no evidence in either of the sexes that genetic trade-offs between heat tolerance and fitness will constrain responses to thermal selection. Our results suggest that neither trade-offs, nor sex-specific genetics, will significantly constrain an evolutionary response to climatic warming, at least in this population of D. melanogaster.

PLoS one, January 2012

DK Dowling, LW Simmons

Trade-offs between investment into male sexual traits and immune function provide the foundation for some of the most prominent models of sexual selection. Post-copulatory sexual selection on the male ejaculate is intense, and therefore tradeoffs should occur between investment into the ejaculate and the immune system. Examples of such trade-offs exist, including that between sperm quality and immunity in the Australian cricket, Teleogryllus oceanicus. Here, we explore the dynamics of this trade-off, examining the effects that increased levels of sexual interaction have on the viability of a male’s sperm across time, and the concomitant effects on immune function. Males were assigned to a treatment, whereby they cohabited with females that were sexually immature, sexually mature but incapable of copulation, or sexually mature and capable of copulation. Sperm viability of each male was then assessed at two time points: six and 13 days into the treatment, and immune function at day 13. Sperm viability decreased across the time points, but only for males exposed to treatment classes involving sexually mature females. This decrease was similar in magnitude across both sexually mature classes, indicating that costs to the expression of high sperm viability are incurred largely through levels of pre-copulatory investment. Males exposed to immature females produced sperm of low viability at both time points. Although we confirmed a weak negative association between sperm viability and lytic activity (a measure of immune response to bacterial infection) at day 13, this relationship was not altered across the mating treatment. Our results highlight that sperm viability is a labile trait, costly to produce, and subject to strategic allocation in these crickets.

Ecology Letters, July 2011

M Almbro, DK Dowling, LW Simmons

Sperm are particularly prone to oxidative damage because they generate reactive oxygen species (ROS), have a high polyunsaturated fat content and a reduced capacity to repair DNA damage. The dietary compounds vitamin E and beta-carotene are argued to have antioxidant properties that help to counter the damaging effects of excess ROS. Here in, we tested the post-copulatory consequences for male crickets (Teleogryllus oceanicus) of dietary intake of these two candidate antioxidants. During competitive fertilisation trials, vitamin E, but not beta-carotene, singularly enhanced sperm competitiveness. However, the diet combining a high vitamin E dose and beta-carotene produced males with the most competitive ejaculates, possibly due to the known ability of beta-carotene to recycle vitamin E. Our results provide support for the idea that these two common dietary compounds have interactive antioxidant properties in vivo, by affecting the outcomes of male reproductive success under competitive conditions.

BMC Evolutionary Biology, July 2011

Magdalena Nystrand, Damian K Dowling and Leigh W Simmons

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 genotypeenvironment interactions can have major implications on the potential for evolutionary responses to selection. 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. Our results show that the genetics underlying phenotypic expression can be complex, contextdependent 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.

Science,May 2011

Paolo Innocenti, Edward H. Morrow and Damian K. Dowling

Mitochondria are maternally transmitted; hence, their genome can only make a direct and adaptive response to selection through females, whereas males represent an evolutionary dead end. In theory, this creates a sex-specific selective sieve, enabling deleterious mutations to accumulate in mitochondrial genomes if they exert male-specific effects. We tested this hypothesis, expressing five mitochondrial variants alongside a standard nuclear genome in Drosophila melanogaster, and found striking sexual asymmetry in patterns of nuclear gene expression. Mitochondrial polymorphism had few effects on nuclear gene expression in females but major effects in males, modifying nearly 10% of transcripts. These were mostly male-biased in expression, with enrichment hotspots in the testes and accessory glands. Our results suggest an evolutionary mechanism that results in mitochondrial genomes harboring male-specific mutation loads.

Evolution, November 2010

G Arnqvist, DK Dowling, P Eady, L Gay, T Tregenza, M Tuda, DJ Hosken

The extent to which mitochondrial DNA (mtDNA) variation is involved in adaptive evolutionary change is currently being reevaluated. In particular, emerging evidence suggests that mtDNA genes coevolve with the nuclear genes with which they interact to form the energy producing enzyme complexes in the mitochondria. This suggests that intergenomic epistasis between mitochondrial and nuclear genes may affect whole-organism metabolic phenotypes. Here, we use crossed combinations of mitochondrial and nuclear lineages of the seed beetle Callosobruchus maculatus and assay metabolic rate under two different temperature regimes. Metabolic rate was affected by an interaction between the mitochondrial and nuclear lineages and the temperature regime. Sequence data suggests that mitochondrial genetic variation has a role in determining the outcome of this interaction. Our genetic dissection of metabolic rate reveals a high level of complexity, encompassing genetic interactions over two genomes, and genotype × genotype × environment interactions. The evolutionary implications of these results are twofold. First, because metabolic rate is at the root of life histories, our results provide insights into the complexity of life-history evolution in general, and thermal adaptation in particular. Second, our results suggest a mechanism that could contribute to the maintenance of nonneutral mtDNA polymorphism.

The American Naturalist, June 2010

DK Dowling, T Meerupati, G Arnqvist

Recent studies have uncovered an abundance of nonneutral cytoplasmic genetic variation within species, which suggests that we should no longer consider the cytoplasm an idle intermediary of evolutionary change. Nonneutrality of cytoplasmic genomes is particularly intriguing, given that these genomes are maternally transmitted. This means that the fate of any given cytoplasmic genetic mutation is directly tied to its performance when expressed in females. For this reason, it has been hypothesized that cytoplasmic genes will coevolve via a sexually antagonistic arms race with the biparentally transmitted nuclear genes with which they interact. We assess this prediction, examining the intergenomic contributions to the costs and benefits of mating in Callosobruchus maculatus females subjected to a mating treatment with three classes (kept virgin, mated once, or forced to cohabit with a male). We find no evidence that the economics of mating are determined by interactions between cytoplasmic genes expressed in females and nuclear genes expressed in males and, therefore, no support for a sexually antagonistic intergenomic arms race. The cost of mating to females was, however, shaped by an interaction between the cytoplasmic and nuclear genes expressed within females. Thus, cytonuclear interactions are embroiled in the economics of mating.

Evolution, May 2010

DK Dowling, M Nystrand, LW Simmons

Explanations for the evolution of polyandry often center on the idea that females garner genetic benefits for their offspring by mating multiply. Furthermore, postcopulatory processes are thought to be fundamental to enabling polyandrous females to screen for genetic quality. Much attention has focused on the potential for polyandrous females to accrue such benefits via a sexy- or good-sperm mechanism, whereby additive variation exists among males in sperm competitiveness. Likewise, attention has focused on an alternative model, in which offspring quality (in this context, the sperm competitiveness of sons) hinges on an interaction between parental haplotypes (genetic compatibility). Sperm competitiveness that is contingent on parental compatibility will exhibit nonadditive genetic variation. We tested these models in the Australian cricket, Teleogryllus oceanicus, using a design that allowed us to partition additive, nonadditive genetic, and parental variance for sperm competitiveness. We found an absence of additive and nonadditive genetic variance in this species, challenging the direct relevance of either model to the evolution of sperm competitiveness in particular, and polyandry in general. Instead, we found maternal effects that were possibly sex-linked or cytoplasmically linked.We also found effects of focal male age on sperm competitiveness, with small increments in age conferring more competitive sperm.

Proceedings of the Royal Society B: Biological Sciences, May 2009

DK Dowling, LW Simmons

Evolutionary theory is firmly grounded on the existence of trade-offs between life-history traits, and recent interest has centred on the physiological mechanisms underlying such trade-offs. Several branches of evolutionary biology, particularly those focusing on ageing, immunological and sexual selection theory, have implicated reactive oxygen species (ROS) as profound evolutionary players. ROS are a highly reactive group of oxygen-containing molecules, generated as common by-products of vital oxidative enzyme complexes. Both animals and plants appear to intentionally harness ROS for use as molecular messengers to fulfil a wide range of essential biological processes. However, at high levels, ROS are known to exert very damaging effects through oxidative stress. For these reasons, ROS have been suggested to be important mediators of the cost of reproduction, and of trade-offs between metabolic rate and lifespan, and between immunity, sexual ornamentation and sperm quality. In this review, we integrate the above suggestions into one life-history framework, and review the evidence in support of the contention that ROS production will constitute a primary and universal constraint in life-history evolution.

Journal of Evolutionary Biology, April 2009

DK Dowling, AA Maklakov, U Friberg, F Hailer

Two genetic models exist to explain the evolution of ageing – mutation accumulation (MA) and antagonistic pleiotropy (AP). Under MA, a reduced intensity of selection with age results in accumulation of late-acting deleterious mutations. Under AP, late-acting deleterious mutations accumulate because they confer beneficial effects early in life. Recent studies suggest that the mitochondrial genome is a major player in ageing. It therefore seems plausible that the MA and AP models will be relevant to genomes within the cytoplasm. This possibility has not been considered previously. We explore whether patterns of covariation between fitness and ageing across 25 cytoplasmic lines, sampled from a population of Drosophila melanogaster, are consistent with the genetic associations predicted under MA or AP. We find negative covariation for fitness and the rate of ageing, and positive covariation for fitness and lifespan. Notably, the direction of these associations is opposite to that typically predicted under AP.

Journal of Evolutionary Biology, November 2008

U Friberg, DK Dowling

Recent studies have advocated a role for mitochondrial DNA (mtDNA) in sperm competition. This is controversial because earlier theory and empirical work suggested that mitochondrial genetic variation for fitness is low. Yet, such studies dealt only with females and did not consider that variation that is neutral when expressed in females, might be non-neutral in males as, in most species, mtDNA is never selected in males. We measured male ability to compete for fertilizations, at young and late ages, across 25 cytoplasms expressed in three different nuclear genetic backgrounds, within a population of Drosophila melanogaster. We found no cytoplasmic (thus no mtDNA) genetic variation for either male offence or offensive sperm competitiveness. This contrasts with previous findings demonstrating cytoplasmic genetic variation for female fitness and female ageing across these same lines. Taken together, this suggests that mitochondrial genes do not contribute to variation in sperm competition at the within-population level.

Trends in Ecology & Evolution, October 2008

DK Dowling, U Friberg, J Lindell

Sequence variation in mitochondrial DNA (mtDNA) was traditionally considered to be selectively neutral. However, an accumulating body of evidence indicates that this assumption is invalid. Furthermore, recent advances indicate that mtDNA polymorphism can be maintained within populations via selection on the joint mitochondrial- nuclear genotype. Here, we review the latest findings that show mitochondrial and cytoplasmic genetic variation for life-history traits and fitness. We highlight the key importance of the mitochondrial-nuclear interaction as a unit of selection and discuss the consequences of mitochondrially encoded fitness effects on several key evolutionary processes. Our goal is to draw attention to the profound, yet neglected, influence of the mitochondrial genome on the fields of ecology and evolution.

Journal of Evolutionary Biology, November 2007

DK Dowling, U Friberg, G Arnqvist

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.

Evolution, January 2007

DK Dowling, KC Abiega, G Arnqvist

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.

Genetics, January 2007

DK Dowling, U Friberg, F Hailer, G Arnqvist

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.

Journal of Evolutionary Biology, January 2007

DK Dowling, AL Nowostawski, G Arnqvist

Sperm competition theory predicts that sperm traits influencing male fertilizing ability will evolve adaptively. However, it has been suggested that some sperm traits may be at least partly encoded by mitochondrial genes. If true, this may constrain the adaptive evolution of such traits because mitochondrial DNA (mtDNA) is maternally inherited and there is thus no selection on mtDNA in males. Phenotypic variation in such traits may nevertheless be high because mutations in mtDNA that have deleterious effects on male traits, but neutral or beneficial effects in females, may be maintained by random processes or selection in females. We used backcrossing to create introgression lines of seed beetles (Callosobruchus maculatus), carrying orthogonal combinations of distinct lineages of cytoplasmic and nuclear genes, and then assayed sperm viability and sperm length in all lines. We found sizeable cytoplasmic effects on both sperm traits and our analyses also suggested that the cytoplasmic effects varied across nuclear genetic backgrounds. We discuss some potential implications of these findings for sperm competition theory.

Evolution, October 2006

AA Maklakov, U Friberg, DK Dowling, G Arnqvist

It has been suggested that mitochondrial DNA (mtDNA) may play an important role in aging. Yet, few empirical studies have tested this hypothesis, partly because the degree of sequence polymorphism in mtDNA is assumed to be low. However, low sequence variation may not necessarily translate into low phenotypic variation. Here, we report an experiment that tests whether there is within-population variation in cytoplasmic genes for female longevity and senescence. To achieve this, we randomly selected 25 ‘‘mitochondrial founders’’ from a single, panmictic population of Drosophila melanogaster and used these founders to generate distinct ‘‘mt’’ lines in which we controlled for the nuclear background by successive backcrossing. Potential confounding effects of cytoplasmically transmitted bacteria were eliminated by tetracycline treatment. The mt lines were then assayed for differences in longevity, Gompertz intercept (frailty), and demographic rate of change in mortality with age (rate-of-senescence) in females. We found significant cytoplasmic effects on all three variables. This provides evidence that genetic variation in cytoplasmic genes, presumably mtDNA, contributes to variation in female mortality and aging.

Annales Zoologici Fennici, August 2006

DK Dowling, RA Mulder

Red plumage is produced mainly by deposition of carotenoid pigments into the feathers and is assumed to be costly. Recent studies suggest red plumage may be a condition-dependent, sexually selected signal. To date, few studies have explored the relationship between carotenoid-based plumage colour and genetic (realised) reproductive success. This is despite the rarity of genetic monogamy among avian mating systems. We studied this relationship in the red-capped robin (Petrioca goodenovii) across two breeding seasons , using spectrophotometric techniques to score colour and molecular markers to assign paternity. Males with the highest within-pair reproductive success during the first season moulted into the most colourful plumage at the conclusion of the season. We found no such correlations when using putative measures of reproductive success, underlining the importance of unambiguous paternity assignment. However, males that moulted into the most colourful plumage did not go on to attain highest reproductive success during the subsequent breeding season (while displaying this plumage). Instead, variation in male reproductive success was explained by male body condition and age. These results suggest that the information value of male plumage colour is unpredicatable.

Journal of Evolutionary Biology, March 2006

DK Dowling, RA Mulder

Sex allocation theory predicts females will adaptively manipulate sex ratios to maximize their progeny’s reproductive value. Recently, the generality of biased sex allocation in birds has been questioned by meta-analytic reviews, which demonstrate that many previously reported significant results may simply reflect sampling error. Here, we utilize a robust sample size and powerful statistical approach to determine whether parental quality is correlated with biased sex allocation in red-capped robins. Indices of maternal quality (including interactive effects of age and condition) were strongly related to sex allocation. These relationships were in the predicted directions, with larger effect sizes than those of previous studies in this field. There were also paternal correlates, involving age and the source of paternity. We propose that biased sex allocation occurs in this species, and is maintained by differing production costs of each sex and genetic benefits to females of producing sons when fertilized by high-quality males.

Behavioral Ecology, April 2005

NE Langmore, RM Kilner, SHM Butchart, G Maurer, NB Davies, A Cockburn, NA Macgregor, A Peters, MJL Magrath, DK Dowling

Exploitation of hosts by brood parasitic cuckoos is expected to stimulate a coevolutionary arms race of adaptations and counteradaptations. However, some hosts have not evolved defenses against parasitism. One hypothesis to explain a lack of host defenses is that the life-history strategies of some hosts reduce the cost of parasitism to the extent that accepting parasitic eggs in the nest is evolutionarily stable. Under this hypothesis, it pays hosts to accept cuckoo eggs if (1) the energetic cost of raising the cuckoo is low, (2) there is time to renest, and (3) clutch size is small.We parasitized the nests of host and nonhost species with nonmimetic model eggs to test whether the evolution of egg recognition by cuckoo hosts could be explained by life-history variables of the host. The most significant factor explaining rates of rejection of model eggs was whether or not a species was a cuckoo host, with hosts rejecting model eggs at a higher rate than nonhosts. Egg-rejection rates were also explained by visibility within the nest and by cuckoo mass. We found little support for the life-history model of egg rejection. Our results suggest that parasitism is always sufficiently costly to select for host defenses and that the evolution of defenses may be limited by proximate constraints such as visibility within the nest. Key words: brood parasitism, coevolution, cowbirds, cuckoos, life-history strategies.

Australian Journal of Zoology, February 2004

DK Dowling

Molecular Ecology Notes, August 2003

DK Dowling, GJ Adcock, RA Mulder

Seven microsatellite loci were isolated and characterized from the red-capped robin Petroica goodenovii , using nonradioactive polymerase chain reaction (PCR)-based techniques to screen an enriched genomic library. Five loci showed no evidence of null alleles and were variable [mean heterozygosity ( H E ) = 0.440, mean number of alleles = 8]. Cross-amplification using primers for microsatellites in Phylloscopus occipitalis and Emberiza schoeniclus yielded another two polymorphic loci. The combined set of five red-capped robin and two cross-amplified loci are suitable for paternity assignment (exclusion probability for seven unlinked loci = 0.9760).

Petroica goodenovii. Emu, October 2003

DK Dowling, M Antos, T Sahlman

Behavioral Ecology and Sociobiology, August 2001

DK Dowling, DS Richardson, J Komdeur

A common assumption of studies examining host-symbiont interactions is that all symbiotic organisms are parasitic. Feather mites are widespread symbionts of birds that do not appear to deplete the host of any vital resources. Instead they feed on the oily secretions that cover the feathers and the detritus caught in these secretions. Therefore, a more logical assumption might be that feather mites are non-parasitic. We investigated whether infestation by a feather mite, Trouessartia sp. (Trouessartiidae), has any detrimental effects on the Seychelles warbler, Acrocephalus sechellensis. Feather mite load was not correlated with body condition. Survivorship of birds per territory was lower for birds with lower mite loads, but this result is explained by these birds also living in low-quality territories with low food availability. The amount of time birds spent grooming was not related to feather mite load and grooming did not decrease following the experimental removal of mites. Additionally, although males groom more than females, they do not have larger mite loads than females. Although this study is largely non-experimental, the combined results indicate that the relationship between these feather mites and the Seychelles warbler is probably benign.

Journal of Avian Biology, December 2001

DK Dowling, DS Richardson, K Blaakmeer, J Komdeur

Many factors may affect symbiont distributions within host populations. Intrinsic factors, such as genotype, body condition and age may account for variations in symbiont loads between individuals. However, abiotic factors may also contribute to variations. We investigated correlates of variation in the number of feather mites, Trouessartia sp. (Trouessartiidae), per individual in the Seychelles Warbler Acrocephalus sechellensis on Cousin Island. Warblers from territories exposed to high levels of salt spray had lower feather mite loads than warblers from territories unaffected by salt spray, and juveniles had higher mite loads than adults. When the effects of salt spray were controlled for statistically, incubating birds had lower mite loads than birds in other stages of reproduction. Thus, an extrinsic and two intrinsic factors contribute to predicting feather mite loads.