Biology subjects

Fowler, K.

Publications and source records attributed to Fowler, K..

9 recordsLinked to original sources

bioRxiv2020

A non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster exhibits antagonistically pleiotropic fitness effects

The amount of genetic variation for fitness within populations tends to exceed that expected under mutation-selection-drift balance. Several mechanisms have been proposed to actively maintain polymorphism and account for this discrepancy, including antagonistic pleiotropy (AP), where allelic variants have opposing effects on different components of fitness. Here we identify a non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster and measure survival and reproductive components of fitness in males and females of replicate lines carrying one or the other allele. Expressing the fruitless region in a hemizygous state we observe a pattern of AP, with one allele resulting in greater reproductive fitness while the other confers greater survival to adulthood. Different fitness effects were observed in an alternative genetic background, suggesting widespread epistatic effects. Our findings link sequence-level variation at a single locus with complex effects on a range of fitness components, thus helping to explain the maintenance of genetic variation for fitness. Transcription factors, such as fruitless, may be prime candidates for targets of balancing selection since they interact with multiple target loci and their associated phenotypic effects.

evolutionary biology↗

bioRxiv2020

Mother's curse is pervasive across a large mito-nuclear Drosophila panel

The maternal inheritance of mitochondrial genomes entails a sex-specific selective sieve, whereby mutations in mitochondrial DNA can only respond to selection acting directly on females. In theory, this enables male-harming mutations to accumulate in mitochondrial genomes if they are neutral, beneficial, or only slightly deleterious to females. Ultimately, this bias could drive the evolution of male-specific mitochondrial mutation loads, an idea known as mothers curse. Earlier work on this hypothesis has mainly used small Drosophila panels, in which naturally-sourced mitochondrial genomes were coupled to an isogenic nuclear background. However, the lack of nuclear genetic variation has precluded robust generalization. Here we test the predictions of mothers curse using a large Drosophila mito-nuclear genetic panel, comprising 9 isogenic nuclear genomes coupled to 9 mitochondrial haplotypes, giving a total of 81 different mito-nuclear genotypes. This enables systematic testing of both mito-nuclear interactions and mitochondrial genetic variance. Following a predictive framework, we performed a screen for wing centroid size, as this trait is highly sexually dimorphic and depends on metabolic function. We confirmed that the trait is sexually dimorphic, and show high levels of mito-nuclear epistasis. Importantly, we report that mitochondrial genetic variance has a greater impact on male versus female Drosophila, in 8 out of the 9 nuclear genetic backgrounds. These results demonstrate that the maternal inheritance of mitochondrial DNA does indeed modulate male life-history traits in a more generalisable way than previously envisaged.

evolutionary biology↗

bioRxiv2019

Ancient DNA reconstructs the genetic legacies of pre-contact Puerto Rico communities

Indigenous peoples have occupied the island of Puerto Rico since at least 3000 B.C. Due to the demographic shifts that occurred after European contact, the origin(s) of these ancient populations, and their genetic relationship to present-day islanders, are unclear. We use ancient DNA to characterize the population history and genetic legacies of pre-contact Indigenous communities from Puerto Rico. Bone, tooth and dental calculus samples were collected from 124 individuals from three pre-contact archaeological sites: Tibes, Punta Candelero and Paso del Indio. Despite poor DNA preservation, we used target enrichment and high-throughput sequencing to obtain complete mitochondrial genomes (mtDNA) from 45 individuals and autosomal genotypes from two individuals. We found a high proportion of Native American mtDNA haplogroups A2 and C1 in the pre-contact Puerto Rico sample (40% and 44%, respectively). This distribution, as well as the haplotypes represented, support a primarily Amazonian South American origin for these populations, and mirrors the Native American mtDNA diversity patterns found in present-day islanders. Three mtDNA haplotypes from pre-contact Puerto Rico persist among Puerto Ricans and other Caribbean islanders, indicating that present-day populations are reservoirs of pre-contact mtDNA diversity. Lastly, we find similarity in autosomal ancestry patterns between pre-contact individuals from Puerto Rico and the Bahamas, suggesting a shared component of Indigenous Caribbean ancestry with close affinity to South American populations. Our findings contribute to a more complete reconstruction of pre-contact Caribbean population history and explore the role of Indigenous peoples in shaping the biocultural diversity of present-day Puerto Ricans and other Caribbean islanders.

genomics↗

bioRxiv2019

Does meiotic drive alter male mate preference?

Male mate preferences have been demonstrated across a range of species, including the Malaysian stalk-eyed fly, Teleopsis dalmanni. This species is subject to SR, an X-linked male meiotic driver, that causes the dysfunction of Y-sperm and the production all female broods. SR is associated with a low frequency inversion spanning most of the X chromosome that causes reduced organismal fitness. While there has been work considering female avoidance of meiotic drive males, the mating decisions of drive-bearing males have not been considered previously. As drive males are of lower genetic quality they may be less able to bear the cost of choice or may experience weaker selection for its maintenance if they are avoided by females. We investigated preference of drive males using binary choice trials. We confirmed that males prefer to mate with large females (indicative of greater fecundity) but found no evidence that the strength of male mate preference differs between drive and standard males. This suggests that the cost of choice does not restrict male reference among drive males. In a further experiment, we found that large eyespan males showed strong preference whereas small eyespan males showed no preference. This is likely to weaken mate preference in drive males, as on average they have reduced eyespan compared to standard males. In this respect, drive males are subject to and exert weak sexual selection.\n\nLay summaryWe studied male mate preference in stalk-eyed flies. This species suffers from meiotic drive, a selfish genetic element that causes a reduction in sperm production and organismal fitness. We predicted that males with meiotic drive would show weak mate preference. Males preferred to mate with large females, but there was no difference in the strength of preference between drive and non-drive males. Males with larger eyespan showed stronger mate preference. Meiotic drive males usually have reduced eyespan so on average they exert weaker sexual selection on females, but this is mediated by eyespan, not genotype per se.

evolutionary biology↗

bioRxiv2019

Meiotic drive reduces egg-to-adult viability in stalk-eyed flies

SR meiotic drive is a selfish genetic element located on the X chromosome in a number of species that causes dysfunction of Y-bearing sperm. SR is transmitted to up to 100% of offspring, causing extreme sex ratio bias. SR in several species is found in a stable polymorphism at a moderate frequency, suggesting there must be strong frequency-dependent selection resisting its spread. We investigate the effect of SR on female and male egg-to-adult viability in the Malaysian stalk-eyed fly, Teleopsis dalmanni. SR meiotic drive in this species is old, and appears to be broadly stable at a moderate (~20%) frequency. We use large-scale controlled crosses to estimate the strength of selection acting against SR in female and male carriers. We find that SR reduces the egg-to-adult viability of both sexes. In females, homozygous females experience greater reduction in viability (sf = 0.242) and the deleterious effects of SR are additive ([h] = 0.511). The male deficit in viability (sm = 0.214) is not different from that in homozygous females. The evidence does not support the expectation that deleterious side-effects of SR are recessive or sex-limited. We discuss how these reductions in egg-to-adult survival, as well as other forms of selection acting on SR, act to maintain SR polymorphism in this species.

evolutionary biology↗

bioRxiv2019

Adaptive maintenance of fertility in the face of meiotic drive

Selfish genetic elements that gain a transmission advantage through the destruction of sperm have grave implications for drive male fertility. In the X-linked SR meiotic drive system of a stalk-eyed fly, we found that drive males have greatly enlarged testes and maintain high fertility despite the destruction of half their sperm, even when challenged with fertilising large numbers of females. Conversely, we observed reduced allocation of resources to the accessory glands that probably explains the lower mating frequency of SR males. Body size and eyespan were also reduced, which are likely to impair viability and pre-copulatory success. We discuss the potential evolutionary causes of these differences between drive and standard males.

evolutionary biology↗

bioRxiv2019

Limits to environmental masking of genetic quality in sexual signals

There is considerable debate over the value of male sexual ornaments as signals of genetic quality. Studies alternately report that environmental variation enhances or diminishes the genetic signal, or leads to crossover where genotypes perform well in one environment but poorly in another. A unified understanding is lacking. We conduct the first experimental test examining the dual effects of distinct low and high genetic quality (inbred versus crossed parental lines) and low, through high, to extreme environmental stress (larval diets) on a condition-dependent male ornament. We find that differences in genetic quality signalled by the ornament (male eyespan in Diasemopsis meigenii stalk-eyed flies) become visible and are amplified under high stress but are overwhelmed in extreme stress environments. Variance among distinct genetic lines increases with environmental stress in both genetic quality classes, but at a slower rate in high quality outcrossed flies. Individual genetic lines generally maintain their ranks across environments, except among high quality lines under low stress conditions, where low genetic variance precludes differentiation between ranks. Our results provide a conceptual advance, demonstrating a unified pattern for how genetic and environmental quality interact. They show when environmental conditions lead to the amplification of differences in signals of genetic quality and thereby enhance the potential indirect genetic benefits gained by female mate choice.

evolutionary biology↗

bioRxiv2017

Sex- and genotype-effects on nutrient-dependent fitness landscapes in Drosophila melanogaster

The sexes perform different reproductive roles and have evolved sometimes strikingly different phenotypes. One focal point of adaptive divergence occurs in the context of diet and metabolism, and males and females of a range of species have been shown to require different nutrients to maximise their fitness. Biochemical analyses in Drosophila melanogaster have confirmed that dimorphism in dietary requirements is associated with molecular sex-differences in metabolite titres. In addition, they also showed significant within-sex genetic variation in the metabolome. To date however, it is unknown whether this metabolic variation translates into differences in reproductive fitness. The answer to this question is crucial to establish whether genetic variation is selectively neutral or indicative of constraints on sex-specific physiological adaptation and optimisation. Here we assay genetic variation in consumption and metabolic fitness effects by screening male and female fitness of thirty D. melanogaster genotypes across four protein-to-carbohydrate ratios. In addition to confirming sexual dimorphism in consumption and fitness, we find significant genetic variation in male and female dietary requirements. Importantly, these differences are not explained by feeding responses and most likely reflect metabolic variation that, in turn, suggest the presence of genetic constraints on metabolic dimorphism.

evolutionary biology↗

bioRxiv2017

Sexual antagonism exerts evolutionarily persistent genomic constraints on sexual differentiation in Drosophila melanogaster

The evolution of sexual dimorphism is constrained by a shared genome, leading to sexual antagonism where different alleles at given loci are favoured by selection in males and females. Despite its wide taxonomic incidence, we know little about the identity, genomic location and evolutionary dynamics of antagonistic genetic variants. To address these deficits, we use sex-specific fitness data from 202 fully sequenced hemiclonal D. melanogaster fly lines to perform a genome-wide association study of sexual antagonism. We identify ~230 chromosomal clusters of candidate antagonistic SNPs. In contradiction to classic theory, we find no clear evidence that the X chromosome is a hotspot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D. melanogaster populations. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D. melanogaster distribution range, indicating widespread and evolutionarily persistent (>10,000 years) genomic constraints. Based on our results, we propose that antagonistic variation accumulates due to constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation.

evolutionary biology↗