ORCID Profile
0000-0002-7268-2173
Current Organisation
Edinburgh Napier University
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Population, Ecological and Evolutionary Genetics | Genetics | Epigenetics (incl. Genome Methylation and Epigenomics) | Evolutionary Impacts of Climate Change | Speciation and Extinction | Quantitative Genetics (incl. Disease and Trait Mapping Genetics)
Publisher: The Royal Society
Date: 27-11-2019
Abstract: Selfish ‘meiotic drive’ alleles are transmitted to more than 50% of offspring, allowing them to rapidly invade populations even if they reduce the fitness of in iduals carrying them. Theory predicts that drivers should either fix or go extinct, yet some drivers defy these predictions by persisting at low, stable frequencies for decades. One possible explanation for this discrepancy is that drivers are especially costly when homozygous, although empirical tests of this idea are rare and equivocal. Here, we measure the fitness of female Drosophila pseudoobscura carrying zero, one or two copies of the X-linked driver s ex ratio ( SR ). SR had strong negative effects on female offspring production and the probability of reproductive failure, and these effects were largely similar across four genetic backgrounds. SR was especially costly when homozygous. We used our fitness measurements to parametrize a population genetic model, and found that the female fitness costs observed here can explain the puzzlingly low allele frequency of SR in nature. We also use the model to show how spatial variation in female mating behaviour, fitness costs of SR and the reduced siring success of SR males can jointly explain the north–south cline in SR frequencies across North America.
Publisher: The Royal Society
Date: 07-2020
Abstract: Assuming that fathers never transmit mitochondrial DNA (mtDNA) to their offspring, mitochondrial mutations that affect male fitness are invisible to direct selection on males, leading to an accumulation of male-harming alleles in the mitochondrial genome (mother's curse). However, male phenotypes encoded by mtDNA can still undergo adaptation via kin selection provided that males interact with females carrying related mtDNA, such as their sisters. Here, using experiments with Drosophila melanogaster carrying standardized nuclear DNA but distinct mitochondrial DNA, we test whether the mitochondrial haplotype carried by interacting pairs of larvae affects survival to adulthood, as well as the fitness of the adults. Although mtDNA had no detectable direct or indirect genetic effect on larva-to-adult survival, the fitness of male and female adults was significantly affected by their own mtDNA and the mtDNA carried by their social partner in the larval stage. Thus, mtDNA mutations that alter the effect of male larvae on nearby female larvae (which often carry the same mutation, due to kinship) could theoretically respond to kin selection. We discuss the implications of our findings for the evolution of mitochondria and other maternally inherited endosymbionts.
Publisher: Wiley
Date: 07-11-2020
DOI: 10.1111/JEB.13549
Abstract: Segregation distorters are selfish genetic elements that subvert Mendelian inheritance, often by destroying gametes that do not carry the distorter. Simple theoretical models predict that distorter alleles will either spread to fixation or stabilize at some high intermediate frequency. However, many distorters have substantially lower allele frequencies than predicted by simple models, suggesting that key sources of selection remain to be discovered. Here, we measured the fitness of Drosophila melanogaster adults and juveniles carrying zero, one or two copies of three different variants of the naturally occurring supergene Segregation Distorter (SD), in order to investigate why SD alleles remain relatively rare within populations despite being preferentially inherited. First, we show that the three SD variants differ in the severity and dominance of the fitness costs they impose on in iduals carrying them. Second, SD-carrying parents produced less fit offspring in some crosses, independent of offspring genotype, indicating that SD alleles can have nongenetic, transgenerational costs in addition to their direct costs. Third, we found that SD carriers sometimes produce a biased offspring sex ratio, perhaps due to off-target effects of SD on the sex chromosomes. Finally, we used a theoretical model to investigate how sex ratio and transgenerational effects alter the population genetics of distorter alleles accounting for these additional costs helps to explain why real-world segregation distorter alleles are rarer than predicted.
Publisher: Cold Spring Harbor Laboratory
Date: 22-09-2021
DOI: 10.1101/2021.09.20.461171
Abstract: Mutations that increase fitness in one sex may decrease fitness in the other. Such “sexually antagonistic” (SA) genetic variants can constrain adaptation and increase variability for fitness components (e.g., survival, fertility, and disease susceptibility). However, detecting SA selection in genomes is immensely challenging, as it requires prohibitively large datasets that combine genomic sequences with in idual fitness measurements. Here, we use genotypic and reproductive success data from ∼250,000 UK Biobank in iduals to comprehensively assess the extent of SA genetic variation in humans. We first develop new theoretical models for signals of SA selection spanning a full generational life cycle—including SA polymorphisms affecting survival, reproductive success and overall fitness. Comparing our models with UK Biobank data, we uncover multiple empirical signals of polygenic SA selection, including sex-differential effects of genetic variants on each fitness component, and positive correlations between sex-differential effects and minor allele frequencies. We show that these signals cannot be explained by simple models of sex differences in purifying selection, or by potential confounders such as population structure and sequence mapping errors. We further show that candidate SA sites disproportionately affect functional genomic regions, including polymorphisms associated with quantitative traits and disease. Finally, we examine historical evolutionary processes affecting candidate SA sites, which are consistent with the drift-dominated dynamics predicted by previous theory. Overall, our results support SA genomic variation in humans and highlight its broader functional and evolutionary consequences.
Publisher: Oxford University Press (OUP)
Date: 28-06-2018
Publisher: Springer Science and Business Media LLC
Date: 15-01-2016
Publisher: Oxford University Press (OUP)
Date: 20-09-2023
Publisher: Cold Spring Harbor Laboratory
Date: 23-03-2021
DOI: 10.1101/2021.03.23.436586
Abstract: Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura . Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. In iduals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry in iduals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipid and glycogen. Finally, polyandry males were less desiccation- and starvation-resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism, and nutrient homeostasis.
Publisher: Springer Science and Business Media LLC
Date: 02-2022
DOI: 10.1007/S00265-022-03139-Z
Abstract: Animals living in large colonies are especially vulnerable to infectious pathogens and may therefore have evolved additional defences. Eusocial insects supplement their physiological immune systems with ‘social immunity’, a set of adaptations that impedes the entrance, establishment, and spread of pathogens in the colony. We here find that honey bee workers ( Apis mellifera ) that had been experimentally immune-challenged with bacterial lipopolysaccharide (LPS) often exited the hive and subsequently died some in iduals were dragged out by other workers, while others appeared to leave voluntarily. In a second experiment, we found that healthy workers treated with surface chemicals from LPS-treated bees were evicted from the hive more often than controls, indicating that immune-challenged bees produce chemical cues or signals that elicit their eviction. Thirdly, we observed pairs of bees under lab conditions, and found that pairs spent more time apart when one member of the pair had received LPS, relative to controls. Our findings suggest that immune-challenged bees altruistically banish themselves, and that workers evict sick in iduals which they identify using olfactory cues, putatively because of (kin) selection to limit the spread of pathogens within colonies. Just as in humans, animals living in large groups must contend with infectious diseases. Social insects such as honey bees have evolved a range of behavioural and organisational defences against disease, collectively termed ‘social immunity’. Here, we describe experiments in which we introduced immune-stimulated bee workers into hives to study social immunity. We find that bees that were wounded or immune-challenged were more likely to leave the hive—resulting in their death—compared to healthy controls. Some of the bees leaving the hive were ejected by other workers, while some left the hive seemingly by choice: we thus find evidence for both ‘banishment’ of immune-challenged bees and self-imposed exile. Furthermore, using experiments transferring chemical signals between healthy and immune stimulated bees, we establish that the latter are identified for banishment by the chemicals present on their body surface.
Publisher: Cold Spring Harbor Laboratory
Date: 22-08-2020
DOI: 10.1101/2020.08.21.262113
Abstract: Animals living in large colonies are especially vulnerable to infectious pathogens, and may there-fore have evolved additional defences. Eusocial insects supplement their physiological immune systems with ‘social immunity’, a set of adaptations that impedes the entrance, establishment, and spread of pathogens in the colony. We here find that honey bee workers ( Apis mellifera ) that had been experimentally immune-challenged with lipopolysaccharide (LPS) often exited the hive and subsequently died some in iduals were dragged out by other workers, while others appeared to leave voluntarily. In a second experiment, we found that healthy workers treated with surface chemicals from LPS-treated bees were evicted from the hive more often than controls, indicating that immune-challenged bees produce chemical cues or signals that elicit their eviction. Thirdly, we observed pairs of bees in the lab, and found that pairs spent more time apart when one member of the pair had received LPS, relative to controls. Our findings suggest that immune-challenged bees altruistically banish themselves, and that workers evict sick in iduals which they identify using olfactory cues, putatively because of (kin) selection to limit the spread of pathogens within colonies.
Publisher: The Royal Society
Date: 09-10-2019
Abstract: Synthetic gene drives may soon be used to suppress or eliminate populations of disease vectors, pathogens, invasive species, and agricultural pests. Recent proposals have focused on using Z -linked gene drives to control species with ZW sex determination, which include Lepidopteran pests, parasitic trematodes, and cane toads. These proposals include Z -linked ‘ W -shredders’, which would suppress populations by cleaving the W chromosome and causing females to produce only sons, as well as Z -linked female-sterilizing gene drives. Here, I use eco-evolutionary simulations to evaluate the potential of some proposed Z -linked gene drives, and to produce recommendations regarding their design and use. The simulations show that W -shredders are likely to be highly effective at eradicating populations provided that resistance to W -shredding cannot evolve. However, W -shredder alleles can invade populations from very low frequencies, making it difficult to eliminate specific populations while leaving nearby populations untouched this issue may restrict their possible uses.
Publisher: Wiley
Date: 15-11-2020
DOI: 10.1111/JEB.13561
Abstract: Maternal inheritance of mitochondrial DNA (mtDNA) was originally thought to prevent any response to selection on male phenotypic variation attributable to mtDNA, resulting in a male-biased mtDNA mutation load ("mother's curse"). However, the theory underpinning this claim implicitly assumes that a male's mtDNA has no effect on the fitness of females he comes into contact with. If such "mitochondrially encoded indirect genetics effects" (mtIGEs) do in fact exist, and there is relatedness between the mitochondrial genomes of interacting males and females, male mtDNA-encoded traits can undergo adaptation after all. We tested this possibility using strains of Drosophila melanogaster that differ in their mtDNA. Our experiments indicate that female fitness is influenced by the mtDNA carried by males that the females encounter, which could plausibly allow the mitochondrial genome to evolve via kin selection. We argue that mtIGEs are probably common, and that this might ameliorate or exacerbate mother's curse.
Publisher: Wiley
Date: 24-09-2020
DOI: 10.1111/JEB.13693
Publisher: Cold Spring Harbor Laboratory
Date: 14-06-2018
DOI: 10.1101/345975
Abstract: Evidence suggests that women in academia are hindered by conscious and unconscious biases, and often feel excluded from formal and informal opportunities for research collaboration. In addition to ensuring fairness and helping to redress gender imbalance in the academic workforce, increasing women’s access to collaboration could help scientific progress by drawing on more of the available human capital. Here, we test whether researchers tend to collaborate with same-gendered colleagues, using more stringent methods and a larger dataset than in past work. Our results reaffirm that researchers co-publish with colleagues of the same gender more often than expected by chance, and show that this ‘gender homophily’ is slightly stronger today than it was 10 years ago. Contrary to our expectations, we found no evidence that homophily is driven mostly by senior academics, and no evidence that homophily is stronger in fields where women are in the minority. Interestingly, journals with a high impact factor for their discipline tended to have comparatively low homophily, as predicted if mixed-gender teams produce better research. We discuss some potential causes of gender homophily in science.
Publisher: Wiley
Date: 07-03-2021
DOI: 10.1111/EVO.14183
Publisher: Wiley
Date: 05-04-2022
DOI: 10.1111/JEB.14003
Abstract: Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life-history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. In iduals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry in iduals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipids and glycogen. Finally, polyandry males were less desiccation- and starvation resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism and nutrient homeostasis.
Publisher: Public Library of Science (PLoS)
Date: 26-04-2019
Publisher: The Royal Society
Date: 29-09-2021
Abstract: The Segregation Distorter ( SD ) allele found in Drosophila melanogaster distorts Mendelian inheritance in heterozygous males by causing developmental failure of non- SD spermatids, such that greater than 90% of the surviving sperm carry SD . This within-in idual advantage should cause SD to fix, and yet SD is typically rare in wild populations. Here, we explore whether this paradox can be resolved by sexual selection, by testing if males carrying three different variants of SD suffer reduced pre- or post-copulatory reproductive success. We find that males carrying the SD allele are just as successful at securing matings as control males, but that one SD variant ( SD-5 ) reduces sperm competitive ability and increases the likelihood of female remating. We then used these results to inform a theoretical model we found that sexual selection could limit SD to natural frequencies when sperm competitive ability and female remating rate equalled the values observed for SD-5 . However, sexual selection was unable to explain natural frequencies of the SD allele when the model was parameterized with the values found for two other SD variants, indicating that sexual selection alone is unlikely to explain the rarity of SD .
Publisher: Wiley
Date: 12-2021
DOI: 10.1111/JEB.13885
Abstract: Inspection of the data that accompany Pruitt and Krauel's study of in idual variation in satiation threshold and a comparison of these data with the Materials and Methods and Results sections of the paper have revealed a number of issues that cast doubts on the reliability of the data and any results based on these data. In particular, we show that, following our analyses, the data are unlikely to have been obtained using the study design outlined in the publication and that statistical analyses of these data provide results that differ in important ways from those reported. These findings illustrate the importance of making raw data and analysis code available for the rigour and reproducibility of the scientific literature.
Publisher: Public Library of Science (PLoS)
Date: 19-04-2018
Publisher: Wiley
Date: 20-08-2017
DOI: 10.1111/JEB.13149
Abstract: The capacity of a population to adapt to selection (evolvability) depends on whether the structure of genetic variation permits the evolution of fitter trait combinations. Selection, genetic variance and genetic covariance can change under environmental stress, and males and females are not genetically independent, yet the combined effects of stress and dioecy on evolvability are not well understood. Here, we estimate selection, genetic (co)variance and evolvability in both sexes of Tribolium castaneum flour beetles under stressful and benign conditions, using a half-sib breeding design. Although stress uncovered substantial latent heritability, stress also affected genetic covariance, such that evolvability remained low under stress. Sexual selection on males and natural selection on females favoured a similar phenotype, and there was positive intersex genetic covariance. Consequently, sexual selection on males augmented adaptation in females, and intralocus sexual conflict was weak or absent. This study highlights that increased heritability does not necessarily increase evolvability, suggests that selection can deplete genetic variance for multivariate trait combinations with strong effects on fitness, and tests the recent hypothesis that sexual conflict is weaker in stressful or novel environments.
Location: United Kingdom of Great Britain and Northern Ireland
Start Date: 06-2014
End Date: 06-2017
Amount: $390,000.00
Funder: Australian Research Council
View Funded ActivityStart Date: 2017
End Date: 12-2020
Amount: $380,000.00
Funder: Australian Research Council
View Funded Activity