Biology subjects

Bridle, J. R.

Publications and source records attributed to Bridle, J. R..

11 recordsLinked to original sources

bioRxiv2022

Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes

Rapid ecological speciation along depth gradients has taken place independently and repeatedly in freshwater fishes. While the extent of genomic divergence between ecomorphs is often well understood, the molecular mechanisms facilitating such rapid diversification are typically unclear. In Lake Masoko, an East African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow littoral and deep benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data from jaw tissue, we explore two major regulatory transcriptional mechanisms, expression and splicing QTL variants and examine their contribution to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 4.2% were regulated by cis-regulatory expression QTLs, and 6.4% were regulated by cis-regulatory splicing QTLs. There were also strong signals of divergent selection of differentially expressed genes that showed divergent regulation from expression, splicing or both QTL variants, including genes associated with major jaw plasticity and adaptation networks, adaptive immune system response, and oxidoreductase processes. These results suggest that transcriptome plasticity and modification have important roles during early-stage ecological speciation and demonstrate the role of regulatory-variants as important targets of selection driving ecologically-relevant divergence in gene expression that is associated with adaptive diversification.

evolutionary biology↗

bioRxiv2021

Predicted responses to selection across the climatic range of a rainforest Drosophila without local adaptation: environmental variation limits trait divergence along ecological gradients

Evolutionary responses to environmental change require heritable variation in traits under selection. Both heritability and selection vary with the environment, and may also covary, so environmental variation can affect evolutionary rates. However, simultaneous estimates of heritability and selection across environmental gradients in the field are rare. We estimated environmental variation in selection on three traits (cold tolerance, heat tolerance, and wing size) of the rainforest fruitfly Drosophila birchii. We transplanted flies in cages along two elevational gradients in north-east Queensland, Australia, and calculated the genetic covariance of trait values with fitness (productivity in cages) at each site. For wing size, we estimated heritability at each site from the correlation between field-reared offspring and their laboratory-reared relatives. We used estimates of selection and heritability to predict selection responses along the elevation gradients, and compared these with trait variation observed in flies sourced from populations at elevational extremes. We found evidence for divergent selection on cold tolerance across elevation at one gradient. Heritability of wing size was highest at gradient ends, and the size of the predicted response to selection on this trait increased with elevation. However, the direction of selection varied, even among adjacent sites, making such selection unlikely to cause divergence of this trait with elevation. None of the traits differed between populations from elevational extremes at either gradient. Variation in the strength and direction of selection over small spatial scales, as well as in time, may explain why predicted responses to selection are often not seen in natural populations.

evolutionary biology↗

bioRxiv2021

Plasticity in novel environments induces larger changes in genetic variance than adaptive divergence

Adaptive plasticity allows populations to cope with environmental variation but is expected to fail as conditions become unfamiliar. In novel conditions, populations may instead rely on rapid adaptation to increase fitness and avoid extinction. Adaptation should be fastest when both plasticity and selection occur in directions of the multivariate phenotype that contain abundant genetic variation. However, tests of this prediction from field experiments are rare. Here, we quantify how additive genetic variance in a multivariate phenotype changes across an elevational gradient, and test whether plasticity and selection align with genetic variation. We do so using two closely related, but ecologically distinct, sister species of Sicilian daisy (Senecio, Asteraceae) adapted to high and low elevations on Mount Etna. Using a paternal half-sibling breeding design, we generated and then reciprocally planted c.19,000 seeds of both species, across an elevational gradient spanning each species native elevation, and then quantified mortality and five leaf traits of emergent seedlings. We found that genetic variance in leaf traits changed more across elevations than between species. The high-elevation species at novel lower elevations showed changes in the distribution of genetic variance among the leaf traits, which reduced the amount of genetic variance in the directions of selection and the native phenotype. By contrast, the low-elevation species mainly showed changes in the amount of genetic variance at the novel high elevation, and genetic variance was concentrated in the direction of the native phenotype. For both species, leaf trait plasticity across elevations was in a direction of the multivariate phenotype that contained a moderate amount of genetic variance. Together, these data suggest that where plasticity is adaptive, selection on genetic variance for an initially plastic response could promote adaptation. However, large environmental effects on genetic variance are likely to reduce adaptive potential in novel environments.

evolutionary biology↗

bioRxiv2021

Adaptive maternal effects in early life history traits help to maintain ecological resilience in novel environments for two contrasting Senecio species

While many organisms shift their development plastically to maintain fitness as environments change, such plasticity has limits. Population mean fitness is expected to decline when novel environments exceed the limits to plasticity, but the level of fitness costs is expected to vary among genotypes that can increase adaptive potential. We lack fundamental insights into how and when changes in early development traits increase adaptive potential in novel environments, which limits our ability to predict the response of natural populations to global change. To test whether genetic variation in development time is associated with increased adaptive potential in novel environments, we used a breeding design to generate c.20,000 seeds of two ecologically contrasting Sicilian species of daisies (Senecio, Asteraceae) adapted to high and low elevations on Mount Etna. We planted the seeds across four elevations that included the native range of each species, and a novel elevation. We tracked seedling mortality and measured development time as the number of days it took seedlings to establish. As predicted, genetic variance in survival increased at novel elevations. However, genetic variance in development time showed the opposite trend, decreasing at novel elevations. A strong negative genetic correlation between development time in the native range and survival at novel elevations suggested that genotypes with faster development in native environments survived better in novel environments. These results were consistent across the two ecologically contrasting species, suggesting that genetic variance in early development in native environments could be used to predict population responses to novel environments.

evolutionary biology↗

bioRxiv2021

Social and physical environment independently affect oviposition decisions in Drosophila melanogaster

In response to environmental stimuli, including variation in the presence of conspecifics, animals show highly plastic responses in behavioural and physiological traits influencing reproduction. These responses have been extensively documented in males, but equivalent study of females is so far lacking. We expect females to be highly responsive to environmental variation, with significant impacts on fitness given females direct impact on offspring number, size, and developmental conditions. Using Drosophila melanogaster as a model, we manipulate (a) exposure to conspecific females, expected to influence their expectation of number of potential mates and larval density for their own offspring, and (b) test how prior consexual population density interacts with the spatial distribution of potential oviposition sites, with females expected to prefer clustered food resources that can support a larger number of eggs and larvae. After exposure to competition, females were slower to start copulating and reduced their copulation duration - the opposite effect to that observed in males previously exposed to rivals. There was a parallel and perhaps related effect on egg production, with females previously housed in groups laying fewer eggs than those that were housed in solitude. The spatial distribution of resources also influenced oviposition behaviour: females clearly preferred aggregated patches of substrate, being more likely to lay, and laying on more of the available patches, in the clustered environment. However, we found no significant interaction between prior housing conditions and resource patchiness, indicating that females did not perceive the value of different resource distributions differently when they were expecting either high or low levels of larval competition. While exposure to consexual competition influences copulatory behaviours, it is the distribution of oviposition resources that has a greater impact on oviposition decisions.

animal behavior and cognition↗

bioRxiv2020

Hidden genetic variation in plasticity increases the potential to adapt to novel environments

Rapid environmental change is forcing populations into novel environments where plasticity will no longer maintain fitness. When populations are exposed to novel environments, evolutionary theory predicts that genetic variation in fitness will increase and should be associated with genetic differences in plasticity. If true, then genetic variation in plasticity can increase adaptive potential in novel environments, and population persistence via rapid adaptation is more likely. To test whether genetic variation in fitness increases in novel environments and is associated with plasticity, we transplanted 8,149 clones of 314 genotypes of a Sicilian daisy (Senecio chrysanthemifolius) within and outside its native range, and quantified genetic variation in fitness, and plasticity in leaf traits and gene expression. Although mean fitness declined by 87% in the novel environment, genetic variance in fitness increased threefold and was correlated with plasticity in leaf traits. High fitness genotypes showed greater plasticity in gene expression, but lower plasticity in most leaf traits. Interestingly, genotypes with greater fitness in the novel environment had the lowest fitness at the native site. These results suggest that standing genetic variation in plasticity could help populations to persist and adapt to novel environments, despite remaining hidden in native environments.

evolutionary biology↗

bioRxiv2020

Haplotype tagging reveals parallel formation of hybrid races in two butterfly species

Genetic variation segregates as linked sets of variants, or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. And yet, genomic data often lack haplotype information, due to constraints in sequencing technologies. Here we present "haplotagging", a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabase-size haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high- and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species the geographic clines for the major wing pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the centre of the hybrid zone. We propose that shared warning signalling (Mullerian mimicry) may couple the cline shifts seen in both species, and facilitate the parallel co-emergence of a novel hybrid morph in both co-mimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations. One-sentence summaryHaplotagging, a novel linked-read sequencing technique that enables whole genome haplotyping in large populations, reveals the formation of a novel hybrid race in parallel hybrid zones of two co-mimicking Heliconius butterfly species through strikingly parallel divergences in their genomes.

evolutionary biology↗

bioRxiv2020

Spatially clustered resources increase aggregation and mating duration in Drosophila melanogaster

In environments where females mate multiply, males should adjust their behaviour and physiology in response to the prevailing perceived level of sperm competition. This expectation is well supported by both laboratory and field studies, but we dont yet know what mechanisms facilitate these plastic responses in natural populations. One way in which males appear to assess sperm competition risk is through encounter rates with conspecific males. Such encounter rates may be driven by the spatial distribution of resources required by male. However, explicit links between resource distribution, male encounter rate, and shifts in behaviour related to sperm competition have not been demonstrated. Here we show that a small increase in the distance of patches of food resources in the laboratory: (a) approximately halves the mean distances between pairs of males; and (b) is associated with an increase in subsequent copulation duration - previously shown to be a reliable indicator of male perception of sperm competition risk - by more than two minutes. Aggregation of resources, operating via increased encounter rate, is a mechanism that can stimulate plastic male sperm competition responses. Because spatial distribution of resources, including those exploited by Drosophila, is variable in nature, this may explain one way in which sperm competition-related plasticity is influenced in wild-living males.

animal behavior and cognition↗

bioRxiv2020

Ecology and evolutionary history determine plastic responses to environmental variation in two closely related species

The evolution of plastic responses to external cues allows species to track the environmental variation they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity is associated with recent adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled c.40 genotypes of each species from natural populations on and around Mt Etna and then reciprocally transplanted multiple clones of each genotype into four field sites along an elevational gradient representing each species native range, the edge of their range, and conditions outside their native range. At each elevation we quantified survival and measured leaf traits that included investment (specific leaf area), morphology, chlorophyll fluorescence, pigment content and gene expression. As evidence of adaptive divergence, both species performed better at their native site and better than the species from the other habitat. Traits and differentially expressed genes that changed with elevation in one species often showed little change in the other species, or changed in the opposite direction. Adaptive divergence is therefore associated with the evolution of distinct plastic responses to environmental variation, despite these two species sharing a recent common ancestor.

evolutionary biology↗

bioRxiv2018

Low but genetically variable male mating ability in a tropical Drosophila despite fitness benefits of remating

Mating success is the main source of fitness variation in males, meaning that males should capitalise on all opportunities for mating. Strong selection on male mating success should also reduce genetic variation in male mating traits relative to other traits. We quantified mating latency, mating duration and productivity in males of the tropical fruitfly, Drosophila birchii, from 30 isofemale lines collected from across two elevational gradients, when they were given opportunities to mate with up to four females consecutively. Male remating rates were low compared to other Drosophila (only 14 - 27% of males achieved a fourth mating), with mean mating durations approximately doubling across successive copulations. However, although successive remating produced progressively fewer offspring, it consistently increased overall male reproductive success, with males that mated four times more than doubling offspring number compared to males mating only once. We also found no reduction in the productivity of sons emerging from later matings, indicating a sustained cumulative fitness benefit to remating. Heritable variation was observed for most traits (H2 = 0.035 - 0.292) except mating latency, but there was no divergence in trait means with elevation. The observed restricted remating ability of male D. birchii, despite the clear benefits of remating, may be due to a low encounter rate with females in the field, leading to high investment per gamete (or ejaculate). However, it remains unclear why genetic variation in these traits is high, given we observe no variation in these traits across elevational gradients known to affect local population density.

evolutionary biology↗

bioRxiv2018

Interacting effects of the abiotic and biotic environment on fitness of rainforest Drosophila

Competition within and between species can have large effects on fitness and may therefore drive local adaptation. However, these effects are rarely tested systematically, or considered when predicting species responses to environmental change. We used a field transplant experiment to test the effects of intra and interspecific competition on fitness across the ecological niches of two rainforest Drosophila species that replace each other along an elevation gradient. For the species with the broader elevational range, we also tested for adaptation to the local abiotic and biotic environment. In both species, intraspecific competition reduced productivity more than interspecific competition at the centre of its elevational range, while interspecific competition had a stronger effect at the range edge, where the competing species is more abundant. Local adaptation was detected in the centre of the range of the more widespread species, but only in the presence of intraspecific competition. This study is the first to demonstrate that fitness effects of inter-specific competition increase at ecological margins, while intra-specific competition has more pervasive effects at range centres. This is a key assumption of "tangled bank" models of community evolution and has important implications for predicting the resilience of ecological networks to global change.

evolutionary biology↗