Evolutionary rescue and the limits to phenotypic plasticity: testing theory in the field
Lead Research Organisation:
University of Oxford
Department Name: Plant Sciences
Abstract
Rapid climate change and habitat loss will cause many species to become extinct this century unless they can cope with changing and more extreme ecological conditions. Understanding what limits species' ecological tolerances is therefore an issue of critical scientific importance because it allows us to predict the consequences of ongoing rates of environmental change to populations and therefore to ecological communities.
A common way that organisms deal with environmental variation is to be 'plastic', i.e. to change their morphological, physiological or behavioural traits (their phenotypes) directly in response to their local environment, without requiring rapid evolutionary change. Such 'phenotypic plasticity' buffers changes in the environment, and can maintain fitness across the range of environments typically experienced by a species. Currently, most of the global responses of biodiversity to climate change have been ascribed to such phenotypic plasticity, rather than to actual evolutionary change, underlining its importance in maintaining ecological outputs.
However, the ability of phenotypic plasticity to cope with environmental change has limits. Not only is maintaining variation in gene expression likely to be energetically expensive, it also evolves to maintain fitness only within the range of environments a species experiences in its recent past. In novel or extreme conditions, there is therefore no reason that a species' plastic responses will still improve their ability to survive and produce offspring. Instead, plastic responses that were adaptive in former environments may actually reduce their fitness in new environments. This idea is especially worrying because it predicts that plasticity will be unable to cope as ecological change continues, leading to sudden population declines as critical environmental limits are exceeded. By contrast, other theoretical models predict that plastic responses will be able to evolve more quickly in novel environments, generating faster evolutionary responses than predicted by laboratory experiments under common garden conditions.
We will test these theoretical predictions by measuring the plastic responses of two ecologically divergent species of ragwort (genus Senecio) to changes in their altitudinal position, both within and outside their prevailing distributions on the slopes of Mount Etna, Sicily. These species, Senecio aethnensis and S. chrysanthemifolius differ in a number of phenotypic traits, as well as in the expression of key genes that are associated with adaptation to different altitudes. We will transplant genotypes of both species into a range of field conditions and monitor their performance and plasticity over a two-year period in order to determine each genotype's response to conditions outside its normal ('home') environment. We will measure growth and development parameters, and reproductive parameters as a measure of each genotype's local fitness, and test the degree to which the declines in fitness expected with changes in altitude are offset by plastic changes in their phenotype and in gene expression.
We predict that although observed plastic responses will keep individuals healthy and productive under their species' usual range of altitudinal conditions, phenotypic responses will no longer be appropriate with altitudinal changes beyond these limits. Such an empirical finding will have important implications for predicting the continued ability of species to respond plastically to climate change. In particular, it will suggest, the rapid evolution will be necessary to prevent population and species' extinction where rates of environmental change exceed prevailing conditions within their geographical range.
A common way that organisms deal with environmental variation is to be 'plastic', i.e. to change their morphological, physiological or behavioural traits (their phenotypes) directly in response to their local environment, without requiring rapid evolutionary change. Such 'phenotypic plasticity' buffers changes in the environment, and can maintain fitness across the range of environments typically experienced by a species. Currently, most of the global responses of biodiversity to climate change have been ascribed to such phenotypic plasticity, rather than to actual evolutionary change, underlining its importance in maintaining ecological outputs.
However, the ability of phenotypic plasticity to cope with environmental change has limits. Not only is maintaining variation in gene expression likely to be energetically expensive, it also evolves to maintain fitness only within the range of environments a species experiences in its recent past. In novel or extreme conditions, there is therefore no reason that a species' plastic responses will still improve their ability to survive and produce offspring. Instead, plastic responses that were adaptive in former environments may actually reduce their fitness in new environments. This idea is especially worrying because it predicts that plasticity will be unable to cope as ecological change continues, leading to sudden population declines as critical environmental limits are exceeded. By contrast, other theoretical models predict that plastic responses will be able to evolve more quickly in novel environments, generating faster evolutionary responses than predicted by laboratory experiments under common garden conditions.
We will test these theoretical predictions by measuring the plastic responses of two ecologically divergent species of ragwort (genus Senecio) to changes in their altitudinal position, both within and outside their prevailing distributions on the slopes of Mount Etna, Sicily. These species, Senecio aethnensis and S. chrysanthemifolius differ in a number of phenotypic traits, as well as in the expression of key genes that are associated with adaptation to different altitudes. We will transplant genotypes of both species into a range of field conditions and monitor their performance and plasticity over a two-year period in order to determine each genotype's response to conditions outside its normal ('home') environment. We will measure growth and development parameters, and reproductive parameters as a measure of each genotype's local fitness, and test the degree to which the declines in fitness expected with changes in altitude are offset by plastic changes in their phenotype and in gene expression.
We predict that although observed plastic responses will keep individuals healthy and productive under their species' usual range of altitudinal conditions, phenotypic responses will no longer be appropriate with altitudinal changes beyond these limits. Such an empirical finding will have important implications for predicting the continued ability of species to respond plastically to climate change. In particular, it will suggest, the rapid evolution will be necessary to prevent population and species' extinction where rates of environmental change exceed prevailing conditions within their geographical range.
Planned Impact
Economy and society - understanding ecological resilience in changing environments
Biologists have a crucial role to play in generating global sustainability in the coming decades. Although storms and weather loom large in the public's imagination, many of the effects of climate change on human economies will be felt through its effects on the productivity of ecosystems and crops.
A key issue addressed by this research (and highlighted as a priority by the 2011 UK White Paper on Biodiversity) is the role within-species plasticity and evolution plays in the resilience of ecosystems and the biological services that they provide. Such limits to adaptive plasticity could cause sudden changes in ecological communities as well as population (and crop yield) declines as plastic tolerances are exceeded beyond critical limits. The research funded by this application will test the hypothesis that plasticity can only be expected to be adaptive within narrow ecological limits for a given species.
Predicting the ability of plasticity to continue to buffer changing and more variable environments is crucial to understanding these effects on productivity, and of benefit for international and national governments, to whom defining dangerous levels of environmental change (for food security and economic stability) is a crucial issue. In terms of plasticity this demands: (1) defining where limits to adaptive plasticity typically are relative to current and future environmental regimes and; (2) understanding whether phenotypic responses to marginal conditions will accelerate or prevent the evolution of wider ecological tolerances for species of key economic importance.
Crop breeders and the agricultural industry
The proposed research uses Asteraceae species as a model system to define regions of the genome that are crucial for adaptation (and plastic responses) to changing temperature, and more efficient water use. As well as providing general lessons for the limits of plasticity to environmental change, these genes may be of specific use for agronomically important plants within the Asteraceae, such as sunflowers, lettuce, chicory, and artichoke. "Plastic" genes (and an understanding of the limits to plasticity) are likely to become increasingly important in the coming century for improving the resilience of crop plants in agricultural environments that will not only to be warmer and drier on average in Europe, but also more variable. Our transcriptomic analysis of field-induced variation will be a first step towards identifying such "plastic" genes.
The general public
Beyond predicting the biological effects of climate change, and in addition to the fundamental interest in the rapid ecological divergence of these iconic plant species on Mount Etna, the issues of phenotypic plasticity explored in this proposal are part of what is often called the "Nature vs nurture" debate. Approaching this topic from a biological perspective, particularly using modern genomic and genetic tools, makes this discussion more nuanced than typically depicted by the popular press. However, we think it's important that the complexity of how genomes interact with their internal and external environments to make phenotypes is appreciated more generally. This is especially important because such interactions underlie important social issues, such as punishment and social cohesion, lifestyle choices, and health care funding and planning.
Biologists have a crucial role to play in generating global sustainability in the coming decades. Although storms and weather loom large in the public's imagination, many of the effects of climate change on human economies will be felt through its effects on the productivity of ecosystems and crops.
A key issue addressed by this research (and highlighted as a priority by the 2011 UK White Paper on Biodiversity) is the role within-species plasticity and evolution plays in the resilience of ecosystems and the biological services that they provide. Such limits to adaptive plasticity could cause sudden changes in ecological communities as well as population (and crop yield) declines as plastic tolerances are exceeded beyond critical limits. The research funded by this application will test the hypothesis that plasticity can only be expected to be adaptive within narrow ecological limits for a given species.
Predicting the ability of plasticity to continue to buffer changing and more variable environments is crucial to understanding these effects on productivity, and of benefit for international and national governments, to whom defining dangerous levels of environmental change (for food security and economic stability) is a crucial issue. In terms of plasticity this demands: (1) defining where limits to adaptive plasticity typically are relative to current and future environmental regimes and; (2) understanding whether phenotypic responses to marginal conditions will accelerate or prevent the evolution of wider ecological tolerances for species of key economic importance.
Crop breeders and the agricultural industry
The proposed research uses Asteraceae species as a model system to define regions of the genome that are crucial for adaptation (and plastic responses) to changing temperature, and more efficient water use. As well as providing general lessons for the limits of plasticity to environmental change, these genes may be of specific use for agronomically important plants within the Asteraceae, such as sunflowers, lettuce, chicory, and artichoke. "Plastic" genes (and an understanding of the limits to plasticity) are likely to become increasingly important in the coming century for improving the resilience of crop plants in agricultural environments that will not only to be warmer and drier on average in Europe, but also more variable. Our transcriptomic analysis of field-induced variation will be a first step towards identifying such "plastic" genes.
The general public
Beyond predicting the biological effects of climate change, and in addition to the fundamental interest in the rapid ecological divergence of these iconic plant species on Mount Etna, the issues of phenotypic plasticity explored in this proposal are part of what is often called the "Nature vs nurture" debate. Approaching this topic from a biological perspective, particularly using modern genomic and genetic tools, makes this discussion more nuanced than typically depicted by the popular press. However, we think it's important that the complexity of how genomes interact with their internal and external environments to make phenotypes is appreciated more generally. This is especially important because such interactions underlie important social issues, such as punishment and social cohesion, lifestyle choices, and health care funding and planning.
Publications
Walter GM
(2022)
Adaptive divergence generates distinct plastic responses in two closely related Senecio species
in Evolution
Walter GM
(2020)
Senecio as a model system for integrating studies of genotype, phenotype and fitness.
in The New phytologist
Walter GM
(2023)
Hidden genetic variation in plasticity provides the potential for rapid adaptation to novel environments.
in The New phytologist
Wong ELY
(2020)
Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna.
in Molecular ecology
Wong ELY
(2023)
The role of recombination landscape in species hybridisation and speciation.
in Frontiers in plant science
| Description | Our pilot study in during year 1 of the project has provided preliminary data to indicate that the low altitude Senecio chrysanthemifolius has a high degree of phenotypic plasticity whereas high altitude S. aethnesis shows little phenotypic plasticity. This is evidenced by high survival rates for S, chrysanthemifolius at all four altitude sites on Mt Etna - 500m, 1000m, 1500m and 2000m - and lower survival rates for S. aethnensis at altitudes below 2000m. These preliminary phenotypic findings have been augmented with transcriptome analyses of controlled (clonal) genotypes for each species grown in replicate (3 genotypes x 3 replicates) at all 4 altitude sites. Results show high levels of gene expression change with altitude change when compared to the 'home' site of each species. Interestingly, the patterns of gene expression change differ between the two species with S. aethnensis showing far more overexpressed genes compared to underexpressed at lower altitudes whereas in S. chrysanthemifolius two numbers of overexpressed and underexpressed are approximately equal. We are currently exploring the genes affected in more detail to determine their putative functions. In conjunction with the transcriptome analyses we have carried out more out more phenotypic analyses and some physiological measurements. In 2018 we also carried out a far more extensive transplant experiment for S. chrysanthemifolius involving a total of 8,146 plants. For each plant we recorded: a. survival and growth data; b. fitness (number of flowers) for 7,078 plants; c. leaf samples for >70% of plants; d. leaf physiological measurements (Dualex instrument) recorded for >70% of plants; e. RNA sampled from 45 genotypes. These data are currently being analysed. A similar experiment is planned for S.aethnensis in 2019 and plants are currently being grown up in preparation for planting in April/May. The data from our work to date (March 2019) is currently being prepared as two papers: 1) "Differential plasticity in two Senecio species adapted to contrasting environments" to be submitted to New Phytologist in June 2019, and 2) "Genetic variance in fitness at ecological margins", to be submitted to Global Change Biology in July 2019. Results to date that will form the basis of these two papers can be summarised as follows: a. Species are highly adapted to their specific habitats b. The species adapted to high altitudes (and volcanic soil) shows strong physiological plasticity, but weaker morphological plasticity. c. There is genetic variation segregating within a species that may allow adaptation to environments outside their home range. d. The benefit of maternal effects is restricted to within a species' home range. e. Within a population, genotypes that are more variable (plastic) have increased fitness outside their home range, with important implications for range margins and environmental change. During 2019 the above papers were submitted - paper 1 is currently under review in New Phytologist (revised title: Adaptation to contrasting habitats underlies distinct plastic responses to environmental variation in two closely related Senecio species) and paper 2 is in press in New Phytologist (revised title: Population variation in early development can determine ecological resilience in response to environmental change) and is reported via the Bristol submission as no one from Oxford is an author. We also published a major review in New Phytologist (invited Tansley Review) in Jan 2020 (recorded as an output): "Senecio as a model system for integrating studies of genotype, phenotype and fitness". Our key findings (Oxford and Bristol) in 2019 are summarised below: 1. Species are highly adapted to their specific habitats 2. The species adapted to high altitudes (and volcanic soil) shows strong physiological plasticity, but weaker morphological plasticity. 3. There is genetic variation segregating within a species that may allow adaptation to environments outside their home range. 4. Such genetic variation has distinct pathways in gene expression and phenotypic plasticity 5. Such genetic variation is removed at early life history stages within the home range, but maintained by fluctuating selection between seasons 6. Fitness trade-offs arise at early and late life history stages, but higher phenotypic plasticity at the seedling stage can help to track the optimum phenotype. 7. Gene expression differences underlie differential fitness outside the home range. 8. Sequence variants underlie these differences in gene expression and so provide a means of relating sequencing variation to changes in fitness. These results are currently being prepared for a series of papers that will be submitted to New Phytologist (2 papers covering 1, 2 + 3, and 7), Science (4, 5, 6), PLoS Genetics (8, 9). The proposed papers are as follows: 1. Title: Adaptation to contrasting habitats underlies distinct plastic responses to environmental variation in two closely related Senecio species. In review at New Phytologist (Key findings 1, 2) 2. Title: Fluctuating selection, adaptive plasticity and evolutionary rescue entwined. Target Journal: Science. Expected submission date: March 2020. (Key findings 3, 4, 5) 3. Title: Adaptive and maladaptive plasticity determine fitness trade-offs within and outside species ranges. Target journal: New Phytologist. Expected submission date: July 2020. (Key Finding 6) 4.Title: Genomic architecture of gene expression differences underlying fitness. Target Journal: PLoS Genetics. Expected submission July/August 2020 (Key findings 7, 8) Summary of data sets collected during the project to date 2017-2019 1. 2017 field transplant of both species (total plants = 2,868) a. Survival, growth and flowering data b. RNA samples for all plants c. Population-level transcriptome assemblies for each species d. 72 RNAseq (75bp PE reads) samples, 36 per species e. Leaf samples for surviving plants (1,676 plants) f. Chlorophyll fluorescence measurements for a subset of genotypes (164 plants) 2. 2017 pilot seed experiment (7,584 seeds) a. Measured seedling emergence and development 3. 2018 Comparing physiology of two Senecio species a. Plant physiology measurements for both species (~72 plants) 4. 2018 field transplant of both species (total plants = 984) a. Survival 5. 2018 field transplant of S. chrysanthemifolius (total plants = 8,146) a. Survival and growth data b. Fitness (number of flowers) for 7,078 plants c. Leaf samples for >70% of plants d. Leaf physiological measurements (Dualex instrument) recorded for >70% of plants e. RNA sampled from 45 genotypes (~405 plants) f. Population level transcriptome assembly for S. chrysanthemifolius g. RNAseq (150bp PE reads) samples for 12 genotypes h. 118 3' QuantSeq (75bp SE reads) samples, 9 per genotype 6. 2019 field transplant of both species as cuttings (total plants = 1,946) a. Survival and growth b. Fitness (number of flowers) c. Leaf samples for most plants d. Leaf physiology (Dualex instrument) for most plants e. Replicate measurements for b-d in Spring and Autumn 2019 f. RNA samples from 12 genotypes per species (288 plants) 7. 2019 field transplant of seeds for both species (total seeds = 20,800) a. Emergence, survival, growth and development recorded b. Leaf samples taken for ~6,500 plants c. Leaf physiology measurements (Dualex) for ~6,500 plants Updated outputs for 2020: Our paper 'Adaptation to contrasting habitats underlies distinct plastic responses to environmental variation in two closely related Senecio species' was rejected by New Phytologist after a 'reject invite resubmission' decision by the handling editor. The data this paper reports has now been combined with data from subsequent field experiments to produce a more extensive paper that will be submitted to Evolution. Our revised list of proposed submissions is as follows: 1. Title: Adaptive divergence generates distinct plastic responses in two closely related Senecio species. To be submitted to Evolution in March 2021 (IF=3.98). Datasets: 1-4 & 6. Key results: a. Species are adapted to their specific habitats b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation 2. Title: Hidden genetic variation in plasticity increases the potential to adapt to novel environments. To be submitted to PLoS Biology in March 2021 (IF=7.1). Dataset: 5. Key results: a. There is genetic variation segregating within a species that may allow adaptation to environments outside their home range. b. Such genetic variation has distinct pathways in gene expression and phenotypic plasticity c. Such genetic variation is removed at early life history stages within the home range, but maintained by fluctuating selection between seasons 3. Title: Adaptive maternal effects in early life history traits help to maintain ecological resilience in novel environments for two contrasting Senecio species. To be submitted to Journal of Evolutionary Biology in March 2021 (IF=2.5). Datasets: 7. Key results: a. Fitness trade-offs arise at early and late life history stages. b. Maternal variation provides adaptive transgenerational plasticity in novel environments c. Selection on maternal variance could promote evolutionary rescue in novel environments 4. Title: Plasticity in novel environments induces larger changes in genetic variance than adaptive divergence. Submitted to The American Naturalist (IF=4.3). Dataset: 7. Key results: a. Additive genetic variation changes more across elevation than it does between species adapted to contrasting habitats. b. Changes in genetic variance across elevation align with plasticity, suggesting that genetic variation in plasticity could determine ecological resilience in novel environments. 5. Title: Mismatches between genetic and phenotypic variance help to identify the potential for adaptation to novel environments. To be submitted to Ecology Letters in April 2021 (IF=8.66). Dataset: 7. Key results: a. Genetic variation changes in response to environment more than phenotypic variation. b. Although genetic variation aligns with selection, phenotypic variation will likely determine the potential for evolutionary rescue. 6. Title: Gene networks and correlated gene expression underlie evolutionary rescue. To be submitted to PLoS Genetics or New Phytologist in May 2021. Dataset: 5. Key results: a. Differential correlation of gene expression and highly-correlated gene networks can be identified among sets of genotypes. b. Differences in these networks correlate with changes in fitness and phenotype beyond a species home range. c. Functional characterization of networks provides hypotheses to explain evolutionary rescue. Despite the challenges of working during a pandemic, all planned field experiments were carried out in 2020 by our collaborators in Catania under remote supervision by PIs Bridle and Hiscock and post-docs Walter and Clark. Lab-based RNA analyses done by post-doc Clark at Oxford. Whilst delivering our objectives in the final year of the project was very challenging because of Covid-19 (post-docs and PI's could not visit/work in Sicily) the team of collaborators at Catania really stepped up and grasped the challenge to great effect. Under the leadership of Professor Antonietta Cristaudo as team of 4-5 field assistants, including the Masters students listed, successfully delivered the two experiments summarized below and because of the 1-year no-cost extension they can extend these experiments and associated data gathering into 2021. This is why I ticked the 'positive' as well as the 'negative' impact of Covid-19 boxes in the Covid-19 impact questionnaire. 2020 experiment 1: field transplant of cuttings generated in the glasshouse (2,432 plants) a. Measured survival, growth, fitness (number of flowers), leaf morphology, leaf pigment content b. RNA samples taken for 76 genotypes (3 clones x 4 sites = 912 samples) 2020 experiment 2: field transplant of cuttings generated in the glasshouse (3,200 plants) a. Measured survival, growth, fitness (number of flowers), leaf morphology, leaf pigment content In 2021, the two no-cost extensions extensions to the grant allowed us to complete all the measurements and analysis for the 2020 experiment 1 outlined above and carry out an additional set of field experiments beyond our original plans. This work was carried out by the Catania 'team' of field assistants lead by Professor Antonietta Cristaudo and MSc student Delia Terranova. Analyses of data were performed by former post-docs Greg Walter (now Monash University, Australia) and James Clark (now University of Bristol) with input from the PIs. The final transcriptomic sequencing was finished in September/October 2021 producing two datasets, analysis of which is ongoing with James Clark and PIs. The two datasets are: 1) 12 genotypes sequenced to produce 150bp paired end reads on an Illumina NovaSeq 6000 platform for genotyping and 2) 72 samples (2 x 3 x 12 genotypes) sequenced to produce 75bp single end reads on an Illumina NextSeq75 platform for differential expression. The no-cost extension also allowed an additional small programme of field experiments carried out by the Catania team supervised remotely by the PIs and Greg Walter. This is summarized below and will strengthen and expand data already gathered that forms the basis of papers in various stages of review, revision and resubmission. Field work performed in 2021: • Phenotypic/morphological data and RNA was sampled from Senecio chrysanthemifolius genotypes grown at all four experimental gardens along the altitudinal gradient on Mount Etna as described below. • In May, parental plant material was collected from genotypes surviving over winter in the experimental gardens and cuttings taken to propagate these genotypes in the glasshouse. During the second half of June plants grown from cuttings were transplanted into the field for two experiments, for a total of 5,632 rooted cuttings of Senecio chrysanthemifolius split between the 4 experimental gardens on Mt Etna. Plants were watered every day for two weeks to facilitate rooting. • Plants were monitored and watered when necessary through July and August to avoid too many mortalities. • Following transplant mortality was recorded every 10 days until October and when necessary genotypes/clones were replaced cuttings held in reserve. From October phenotypic/morphological traits were measured together with measurements of morpho-physiological traits using Dualex; at this time leaves were also sampled for RNA-analysis. These data are currently being analysed by Greg Walter, James Clark and the PIs. 2021 update on publications: 1. Our paper 'Adaptive divergence generates distinct plastic responses in two closely related Senecio species' has been accepted by Evolution and will be published in 2022. Key findings: a. Species are adapted to their specific habitats; b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation. The status of the other submissions identified in the 2020 report are as follows: 2. Title: Hidden genetic variation in plasticity increases the potential to adapt to novel environments. This was rejected by PLoS Biology and then by Ecology Letters. It is currently in review with Current Biology. Key results: a. There is genetic variation segregating within a species that may allow adaptation to environments outside their home range. b. Such genetic variation has distinct pathways in gene expression and phenotypic plasticity c. Such genetic variation is removed at early life history stages within the home range, but maintained by fluctuating selection between seasons 3. Title: Adaptive maternal effects in early life history traits help to maintain ecological resilience in novel environments for two contrasting Senecio species. Submitted to Journal of Evolutionary Biology and awaiting decision Key results: a. Fitness trade-offs arise at early and late life history stages. b. Maternal variation provides adaptive transgenerational plasticity in novel environments c. Selection on maternal variance could promote evolutionary rescue in novel environments 4. Title: Plasticity in novel environments induces larger changes in genetic variance than adaptive divergence. Revised and then rejected by The American Naturalist. We are revising to send to Proc RSoc B. Key results: a. Additive genetic variation changes more across elevation than it does between species adapted to contrasting habitats. b. Changes in genetic variance across elevation align with plasticity, suggesting that genetic variation in plasticity could determine ecological resilience in novel environments. 5. Title: Mismatches between genetic and phenotypic variance help to identify the potential for adaptation to novel environments. A revised version of this paper with additional new data will be submitted to Ecology Letters. Key results: a. Genetic variation changes in response to environment more than phenotypic variation. b. Although genetic variation aligns with selection, phenotypic variation will likely determine the potential for evolutionary rescue. 6. Title: Gene networks and correlated gene expression underlie evolutionary rescue. Data analysis is still ongoing because of additional new datasets from 2020 and 2021. We still intend to submit to PLoS Genetics or New Phytologist. Key results: a. Differential correlation of gene expression and highly-correlated gene networks can be identified among sets of genotypes. b. Differences in these networks correlate with changes in fitness and phenotype beyond a species home range. c. Functional characterization of networks provides hypotheses to explain evolutionary rescue. |
| Exploitation Route | Our findings to date will be very useful to scientists working on adaptation and plasticity responses to climate change. |
| Sectors | Environment,Other |
| Title | 1. 2017 field transplant of both species (total plants = 2,868) |
| Description | a. Survival, growth and flowering data b. RNA samples for all plants c. Leaf samples for surviving plants (1,676 plants) d. Chlorophyll fluorescence measurements for a subset of genotypes (164 plants) e. RNAseq (75bp PE) from 6 genotypes (72 plants) |
| Type Of Material | Database/Collection of data |
| Year Produced | 2018 |
| Provided To Others? | No |
| Impact | These databases have contributed to the following paper to be submitted shortly Title: Adaptive divergence generates distinct plastic responses in two closely related Senecio species. To be submitted to Evolution in March 2021 (IF=3.98). Datasets: 1-4 & 6. Key results: a. Species are adapted to their specific habitats b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation |
| Title | 12 genotypes sequenced to produce 150bp paired end reads on an Illumina NovaSeq 6000 platform for genotyping |
| Description | 12 genotypes sequenced to produce 150bp paired end reads on an Illumina NovaSeq 6000 platform for genotyping |
| Type Of Material | Database/Collection of data |
| Year Produced | 2021 |
| Provided To Others? | No |
| Impact | None yet but will contribute data to a paper |
| Title | 2. 2017 pilot seed experiment (7,584 seeds) |
| Description | a. Measured seedling emergence and development |
| Type Of Material | Database/Collection of data |
| Year Produced | 2018 |
| Provided To Others? | No |
| Impact | These data have contributed to the following paper to be submitted shortly: 3. Title: Adaptive divergence generates distinct plastic responses in two closely related Senecio species. To be submitted to Evolution in March 2021 (IF=3.98). Datasets: 1-4 & 6. Key results: a. Species are adapted to their specific habitats b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation |
| Title | 3. 2018 Comparing physiology of two Senecio species |
| Description | a. Plant physiology measurements for both species (~72 plants) |
| Type Of Material | Database/Collection of data |
| Year Produced | 2018 |
| Provided To Others? | No |
| Impact | These data have contributed to the following paper to be submitted shortly: 3. Title: Adaptive divergence generates distinct plastic responses in two closely related Senecio species. To be submitted to Evolution in March 2021 (IF=3.98). Datasets: 1-4 & 6. Key results: a. Species are adapted to their specific habitats b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation |
| Title | 4. 2018 field transplant of both species (total plants = 984) |
| Description | a. Survival rates |
| Type Of Material | Database/Collection of data |
| Year Produced | 2018 |
| Provided To Others? | No |
| Impact | These data have contributed to the following paper to be submitted soon: Adaptive divergence generates distinct plastic responses in two closely related Senecio species. To be submitted to Evolution in March 2021 (IF=3.98). Datasets: 1-4 & 6. Key results: a. Species are adapted to their specific habitats b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation |
| Title | 5. 2018 field transplant of S. chrysanthemifolius (total plants = 8,146) |
| Description | a. Survival and growth data b. Fitness (number of flowers) for 7,078 plants c. Leaf samples for >70% of plants d. Leaf physiological measurements (Dualex instrument) recorded for >70% of plants e. RNA sampled from 45 genotypes (~405 plants) f. 3' QuantSeq (75bp SE) and RNAseq (150bp PE) for 12 genotypes (108 plants) |
| Type Of Material | Database/Collection of data |
| Year Produced | 2019 |
| Provided To Others? | No |
| Impact | These data have contributed to the following papers that will be submitted shortly: Hidden genetic variation in plasticity increases the potential to adapt to novel environments. To be submitted to PLoS Biology in March 2021 (IF=7.1). Dataset: 5. Key results: a. There is genetic variation segregating within a species that may allow adaptation to environments outside their home range. b. Such genetic variation has distinct pathways in gene expression and phenotypic plasticity c. Such genetic variation is removed at early life history stages within the home range, but maintained by fluctuating selection between seasons Gene networks and correlated gene expression underlie evolutionary rescue. To be submitted to PLoS Genetics or New Phytologist in May 2021. Dataset: 5. Key results: a. Differential correlation of gene expression and highly-correlated gene networks can be identified among sets of genotypes. b. Differences in these networks correlate with changes in fitness and phenotype beyond a species home range. c. Functional characterization of networks provides hypotheses to explain evolutionary rescue. |
| Title | 6. 2019 field transplant of both species as cuttings (total plants = 1,946) |
| Description | a. Survival and growth b. Fitness (number of flowers) c. Leaf samples for most plants d. Leaf physiology (Dualex instrument) for most plants e. Replicate measurements for b-d in Spring and Autumn 2019 f. RNA samples from 12 genotypes per species (144 plants) g. 3' QuantSeq (75bp SE) and RNAseq (150bp PE) for 12 genotypes per species (216 plants) sampled in Summer 2019 h. 3' QuantSeq (75bp SE) for 6 genotypes per species (54 plants) sampled in Autumn 2019 |
| Type Of Material | Database/Collection of data |
| Year Produced | 2019 |
| Provided To Others? | No |
| Impact | These data have contributed to the following paper due for submission in 2021: Title: Adaptive divergence generates distinct plastic responses in two closely related Senecio species. To be submitted to Evolution in March 2021 (IF=3.98). Datasets: 1-4 & 6. Key results: a. Species are adapted to their specific habitats b. The two species show distinct forms of plasticity as different changes in phenotype and gene expression across elevation |
| Title | 7. 2019 field transplant of seeds for both species (total seeds = 20,800) |
| Description | a. Emergence, survival, growth and development recorded b. Leaf samples taken for ~6,500 plants c. Leaf physiology measurements (Dualex) for ~6,500 plants |
| Type Of Material | Database/Collection of data |
| Year Produced | 2019 |
| Provided To Others? | No |
| Impact | These data form the basis of three papers due for submission in 2021: Title: Adaptive maternal effects in early life history traits help to maintain ecological resilience in novel environments for two contrasting Senecio species. To be submitted to Journal of Evolutionary Biology in March 2021 (IF=2.5). Datasets: 7. Key results: a. Fitness trade-offs arise at early and late life history stages. b. Maternal variation provides adaptive transgenerational plasticity in novel environments c. Selection on maternal variance could promote evolutionary rescue in novel environments Title: Plasticity in novel environments induces larger changes in genetic variance than adaptive divergence. Submitted to The American Naturalist (IF=4.3). Dataset: 7. Key results: a. Additive genetic variation changes more across elevation than it does between species adapted to contrasting habitats. b. Changes in genetic variance across elevation align with plasticity, suggesting that genetic variation in plasticity could determine ecological resilience in novel environments. Title: Mismatches between genetic and phenotypic variance help to identify the potential for adaptation to novel environments. To be submitted to Ecology Letters in April 2021 (IF=8.66). Dataset: 7. Key results: a. Genetic variation changes in response to environment more than phenotypic variation. b. Although genetic variation aligns with selection, phenotypic variation will likely determine the potential for evolutionary rescue. |
| Title | 72 samples (2 x 3 x 12 genotypes) sequenced to produce 75bp single end reads on an Illumina NextSeq75 platform for differential expression |
| Description | 72 samples (2 x 3 x 12 genotypes) sequenced to produce 75bp single end reads on an Illumina NextSeq75 platform for differential expression |
| Type Of Material | Database/Collection of data |
| Year Produced | 2021 |
| Provided To Others? | No |
| Impact | No impact yet - data will contribute to a paper |
| Title | 8. 2020 experiment 1: field transplant of cuttings generated in the glasshouse (2,432 plants) |
| Description | a. Measured survival, growth, fitness (number of flowers), leaf morphology, leaf pigment content b. RNA samples taken for 76 genotypes (3 clones x 4 sites = 912 samples) |
| Type Of Material | Database/Collection of data |
| Year Produced | 2020 |
| Provided To Others? | No |
| Impact | A paper from these data is currently being drafted. |
| Title | 9. 2020 experiment 2: field transplant of cuttings generated in the glasshouse (3,200 plants) |
| Description | a. Measured survival, growth, fitness (number of flowers), leaf morphology, leaf pigment content |
| Type Of Material | Database/Collection of data |
| Year Produced | 2020 |
| Provided To Others? | No |
| Impact | A paper based on these data is currently being drafted. |
| Title | Adaptive divergence generates distinct plastic responses in two closely related Senecio species |
| Description | The evolution of plastic responses to external cues allows species to maintain fitness in response to the environmental variation 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 c.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 change 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. |
| Type Of Material | Database/Collection of data |
| Year Produced | 2022 |
| Provided To Others? | Yes |
| Impact | The dataset resulted in the submission and publication of a paper in Evolution (see outputs section). |
| URL | http://datadryad.org/stash/dataset/doi:10.5061/dryad.9w0vt4bhb |
| Description | Co-supervision of Masters student, Delia Terranova, at the University of Catania. |
| Organisation | University of Catania |
| Country | Italy |
| Sector | Academic/University |
| PI Contribution | I am advising on experimental field work and providing supervision with Professor Cristaudo, Professor Cozzolino, Dr Bridle and Dr Walter. |
| Collaborator Contribution | The University of Catania is providing laboratory and office space for the project and providing transport support and glasshouse support. |
| Impact | Masters Thesis has been completed and the MSc has been awarded. I paper is in preparation from the work. Delia is now doing a PhD with Professor Salvatore Cozzolino at the University of Naples. |
| Start Year | 2018 |
| Description | Co-supervision of Masters student, Giuseppe Emma, at the University of Catania, Sicily. |
| Organisation | University of Catania |
| Country | Italy |
| Sector | Academic/University |
| PI Contribution | Post-doc James Clark and I have been providing advice and guidance in experiment design and planning along with Drs Greg Walter and Jon Bridle, University of Bristol and Professor Antonietta Cristaudo, University of Catania. |
| Collaborator Contribution | The student is conducting field experiments linked to this grant as part of his Masters degree. Specifically, these experiments will involve: 1.) transplant of cuttings derived from specific crosses (projected plant total = 1,728) and 2.) transplant of cuttings of specific genotypes (projected plant total = 3,200) in April/May 2020 followed by phenotypic measurements from then until November. |
| Impact | No outputs so far - too early |
| Start Year | 2019 |
| Description | Co-supervision of PhD student Delia Terranova |
| Organisation | University of Naples |
| Country | Italy |
| Sector | Academic/University |
| PI Contribution | I am co-supervising this PhD. professor Salvatore Cozzolino is the main supervisor. |
| Collaborator Contribution | My partner is the main supervisor |
| Impact | There are no outputs yet. The collaboration is not multi-disciplinary |
| Start Year | 2022 |
| Description | Collaboration with Piante Faro |
| Organisation | Piante Faro |
| Country | Italy |
| Sector | Private |
| PI Contribution | We have provided advice on the identification and cultivation of endemic plants of Mt Etna. We have helped promote Piante Faro at their Garden Festival in 2017. Members of the Faro family will visit Oxford in 2018 to discuss a possible collaboration at Chelsea Flower show. |
| Collaborator Contribution | Piante Faro have provided us with significant plant growing facilities in their glasshouses. Their staff are maintaining our plants and taking cuttings and raising clonal plant material for us. |
| Impact | Piante Faro produced 5000 plants from cuttings for us. They are also maintaining plants for us in their glasshouses free of charge. |
| Start Year | 2017 |
| Description | Collaboration with University of Catania |
| Organisation | University of Catania |
| Country | Italy |
| Sector | Academic/University |
| PI Contribution | We will make a financial contribution from the grant (see JeS forms) of approx £60,000 towards technical assistance, glasshouse space, laboratory space and transport in Sicily. |
| Collaborator Contribution | Our collaborators will also provide in kind contributions of student field assistants and local volunteer help with plant maintenance. Professor Antonietta Cristaudo and Dr Stefania Catara are now working closely with our post-doc Dr Greg Walter who is based in Catania. Professor Cristaudo was responsible for establishing our very valuable collaboration with the commercial nursery Piante Faro in Catania, who are very generously growing and maintaining plants for us at no charge. |
| Impact | The grant commenced in May 2017 with the appointment of Dr Greg Walter as post-doc responsible for managing the field work on Mt Etna. Dr Walter is working on a daily basis with Professor Antonietta Cristaudo and Dr Stefania Catara of Catania University. In year 1 we have established 4 common transplant gardens on Mt Etna at altitudes of 500m, 1000m, 1500m and 2000m. We have also conducted a pilot experiment growing replicated clones of genotypes of Senecio aethnensis (high altitude species 2000m) and S. chrysanthemifoilus (low altitude species 500m) at all 4 transplant gardens. Quantitative trait measurements have been made for all plants and RNA extracted for transcriptome analysis at Oxford. |
| Start Year | 2017 |
| Description | Collaboration with the University of Bristol, School of Biological Sciences (Dr Jon Bridle) |
| Organisation | University of Bristol |
| Department | School of Biological Sciences |
| Country | United Kingdom |
| Sector | Academic/University |
| PI Contribution | Dr Bridle is the Bristol PI and I am the Oxford PI on NERC grant 'Evolutionary rescue and the limits of phenotypic plasticity: testing theory in the field' |
| Collaborator Contribution | We co-wrote the application and are supervising the field work on Mount Etna, Sicily. The project began in May 2017. |
| Impact | Dr Bridle and I have supervised a post-doc (Dr Greg Walter) currently based in Catania, Sicily. Dr Walter began work on the project at the end of May 2017. He is also working with our University of Catania collaborators Professor Antonietta Cristaudo and Dr Stefania Catara and our University of Napoli collaborator Professor Salvatore Cozzolino. In year 1 we have established 4 common transplant gardens on Mt Etna at altitudes of 500m, 1000m, 1500m and 2000m. We have also conducted a pilot experiment growing replicated clones of genotypes of Senecio aethnensis (high altitude species 2000m) and S. chrysanthemifoilus (low altitude species 500m) at all 4 transplant gardens. Quantitative trait measurements have been made for all plants and RNA extracted for transcriptome analysis at Oxford. |
| Start Year | 2016 |
| Description | Collaboration with the University of Napoli (Professor Salvatore Cozzolino) |
| Organisation | University of Naples |
| Country | Italy |
| Sector | Academic/University |
| PI Contribution | We are working closely with Professor Cozzolino on the strategic planning and implementation of the fieldwork on Mt Etna. We have helped Professor Cozzolino set up a 'spin off' collaboration with his colleagues in Bulgaria at the University of Sofia. |
| Collaborator Contribution | Professor Cozzolino is helping to supervise the fieldwork on Mt Etna and is providing a 'language bridge' between us and our collaborators in Catania. Professor Cozzolino has made four trips to Catania/Mt Etna so far spending a total of 2 weeks on the project in the first year. |
| Impact | No concrete outputs yet apart from setting up the field sites on Mt Etna and initiation of first field transplant experiments. Professor Cozzolino was very important in negotiating our collaboration with the commercial nursery Piante Faro. |
| Start Year | 2017 |