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"Bridle, Jon"
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Climate-induced phenology shifts linked to range expansions in species with multiple reproductive cycles per year
Advances in phenology (the annual timing of species’ life-cycles) in response to climate change are generally viewed as bioindicators of climate change, but have not been considered as predictors of range expansions. Here, we show that phenology advances combine with the number of reproductive cycles per year (voltinism) to shape abundance and distribution trends in 130 species of British Lepidoptera, in response to ~0.5 °C spring-temperature warming between 1995 and 2014. Early adult emergence in warm years resulted in increased within- and between-year population growth for species with multiple reproductive cycles per year (
n
=
39 multivoltine species). By contrast, early emergence had neutral or negative consequences for species with a single annual reproductive cycle (
n
= 91 univoltine species), depending on habitat specialisation. We conclude that phenology advances facilitate polewards range expansions in species exhibiting plasticity for both phenology and voltinism, but may inhibit expansion by less flexible species.
Many species’ life cycles have moved earlier in the year because of climate change, but we do not know the consequences for range expansions. The authors show that these advances promote range expansions in species with multiple reproductive cycles per year, but not in species with only one.
Journal Article
Population variation in early development can determine ecological resilience in response to environmental change
• As climate change transforms seasonal patterns of temperature and precipitation, germination success at marginal temperatures will become critical for the long-term persistence of many plant species and communities. If populations vary in their environmental sensitivity to marginal temperatures across a species’ geographical range, populations that respond better to future environmental extremes are likely to be critical for maintaining ecological resilience of the species.
• Using seeds from two to six populations for each of nine species of Mediterranean plants, we characterized patterns of among-population variation in environmental sensitivity by quantifying genotype-by-environment interactions (G × E) for germination success at temperature extremes, and under two light regimes representing conditions below and above the soil surface.
• For eight of nine species tested at hot and cold marginal temperatures, we observed substantial among-population variation in environmental sensitivity for germination success, and this often depended on the light treatment. Importantly, different populations often performed best at different environmental extremes.
• Our results demonstrate that ongoing changes in temperature regime will affect the phenology, fitness, and demography of different populations within the same species differently. We show that quantifying patterns of G × E for multiple populations, and understanding how such patterns arise, can test mechanisms that promote ecological resilience.
Journal Article
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. Yet, genomic data often omit haplotype information due to constraints in sequencing technologies. Here, we present “haplotagging,” a simple, low-cost linkedread 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 center of the hybrid zone. We propose that shared warning signaling (Müllerian mimicry) may couple the cline shifts seen in both species and facilitate the parallel coemergence of a novel hybrid morph in both comimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations.
Journal Article
Local adaptation stops where ecological gradients steepen or are interrupted
Population genetic models of evolution along linear environmental gradients cannot explain why adaptation stops at ecological margins. This is because, unless models impose reductions in carrying capacity at species’ edges, the dominant effect of gene flow is to increase genetic variance and adaptive potential rather than swamping local adaptation. This allows the population to match even very steep changes in trait optima. We extend our previous simulations to explore two nonlinear models of ecological gradients: (a) a sigmoid (steepening) gradient and (b) a linear gradient with a flat centre of variable width. We compare the parameter conditions that allow local adaptation and range expansion from the centre, with those that permit the persistence of a perfectly adapted population distributed across the entire range. Along nonlinear gradients, colonization is easier, and extinction rarer, than along a linear gradient. This is because the shallow environmental gradient near the range centre does not cause gene flow to increase genetic variation, and so does not result in reduced population density. However, as gradient steepness increases, gene flow inflates genetic variance and reduces local population density sufficiently that genetic drift overcomes local selection, creating a finite range margin. When a flat centre is superimposed on a linear gradient, gene flow increases genetic variation dramatically at its edges, leading to an abrupt reduction in density that prevents niche expansion. Remarkably local interruptions in a linear ecological gradient (of a width much less than the mean dispersal distance) can prevent local adaptation beyond this flat centre. In contrast to other situations, this effect is stronger and more consistent where carrying capacity is high. Practically speaking, this means that habitat improvement at patch margins will make evolutionary rescue more likely. By contrast, even small improvements in habitat at patch centres may confine populations to limited areas of ecological space.
Journal Article
Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes
Abstract
Rapid ecological speciation along depth gradients has taken place repeatedly in freshwater fishes, yet molecular mechanisms facilitating such diversification are typically unclear. In Lake Masoko, an 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, we explore two major regulatory transcriptional mechanisms, expression and splicing-QTL variants, and examine their contributions to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 5.4% were regulated by cis-regulatory expression QTLs, and 9.2% were regulated by cis-regulatory splicing QTLs. We also found strong signals of divergent selection on differentially expressed genes associated with craniofacial development. These results suggest that large-scale transcriptome modification plays an important role during early-stage speciation. We conclude that regulatory variants are important targets of selection driving ecologically relevant divergence in gene expression during adaptive diversification.
Journal Article
Adaptive divergence generates distinct plastic responses in two closely related Senecio species
The evolution of plastic responses to external cues allows species to maintain fitness in response to the environmental variations they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity are associated with adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled 40 representative genotypes of each species from their native range on Mt. Etna and then reciprocally transplanted multiple clones of each genotype into four field sites along an elevational gradient that included the native elevational range of each species, and two intermediate elevations. At each elevation, we quantified survival and measured leaf traits that included investment (specific leaf area), morphology, chlorophyll fluorescence, pigment content, and gene expression. Traits and differentially expressed genes that changed with elevation in one species often showed little changes in the other species, or changed in the opposite direction. As evidence of adaptive divergence, both species performed better at their native site and better than the species from the other habitat. Adaptive divergence is, therefore, associated with the evolution of distinct plastic responses to environmental variation, despite these two species sharing a recent common ancestor.
Journal Article
Senecio as a model system for integrating studies of genotype, phenotype and fitness
Two major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype, and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype, and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories, and morphologies, and they occupy a multitude of environments. Common within the genus are species that have hybridized naturally, undergone polyploidization, and colonized diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology.
Journal Article
Evolution on the move: specialization on widespread resources associated with rapid range expansion in response to climate change
Generalist species and phenotypes are expected to perform best under rapid environmental change. In contrast to this view that generalists will inherit the Earth, we find that increased use of a single host plant is associated with the recent climate-driven range expansion of the UK brown argus butterfly. Field assays of female host plant preference across the UK reveal a diversity of adaptations to host plants in long-established parts of the range, whereas butterflies in recently colonized areas are more specialized, consistently preferring to lay eggs on one host plant species that is geographically widespread throughout the region of expansion, despite being locally rare. By common-garden rearing of females’ offspring, we also show an increase in dispersal propensity associated with the colonization of new sites. Range expansion is therefore associated with an increase in the spatial scale of adaptation as dispersive specialists selectively spread into new regions. Major restructuring of patterns of local adaptation is likely to occur across many taxa with climate change, as lineages suited to regional colonization rather than local success emerge and expand.
Journal Article
What is the role of scientists in meeting the environmental challenges of the twenty-first century?
We live at a time of rapid and accelerating biodiversity loss and climate change that pose an existential risk to the environment, humanity, and social justice and stability. Governmental responses are seen by many citizens, including scientists, as inadequate, leading to an increase in civil protests and activism by those calling for urgent action to effect change. Here we consider the role(s) of scientists in responding to those challenges and engaging with policy given that when a scientist moves into political advocacy, reflecting their values and preferences, their objectivity and the value of scientific opinion may be seen as compromised. We then consider whether institutional setting and career stage may affect decisions to engage with policy or activism. Against this backcloth, we ask whether it is sufficient for scientists to act as impartial ‘brokers’ in societal decisions, arguing they should consider acting as ‘ Honest Advocates ’ in policy formation in some circumstances. Such advocacy can contribute to decision-making in a purposeful, well-informed manner, doing societal good without damaging the reputation of science. We encourage scientists to each reflect on their multiple roles in addressing the environmental challenges of our time.
Journal Article