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Lee, G., Sanderson, B. J., Ellis, T. J., Dilkes, B. P., McKay, J. K., Ågren, J. & Oakley, C. G. (2024). A large-effect fitness trade-off across environments is explained by a single mutation affecting cold acclimation. Proceedings of the National Academy of Sciences of the United States of America, 121(6), Article ID e2317461121.
Open this publication in new window or tab >>A large-effect fitness trade-off across environments is explained by a single mutation affecting cold acclimation
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2024 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 121, no 6, article id e2317461121Article in journal (Refereed) Published
Abstract [en]

Identifying the genetic basis of local adaptation and fitness trade-offs across environments is a central goal of evolutionary biology. Cold acclimation is an adaptive plastic response for surviving seasonal freezing, and costs of acclimation may be a general mechanism for fitness trade-offs across environments in temperate zone species. Starting with locally adapted ecotypes of Arabidopsis thaliana from Italy and Sweden, we examined the fitness consequences of a naturally occurring functional polymorphism in CBF2. This gene encodes a transcription factor that is a major regulator of cold-acclimated freezing tolerance and resides within a locus responsible for a genetic trade-off for long-term mean fitness. We estimated the consequences of alternate genotypes of CBF2 on 5-y mean fitness and fitness components at the native field sites by comparing near-isogenic lines with alternate genotypes of CBF2 to their genetic background ecotypes. The effects of CBF2 were validated at the nucleotide level using gene-edited lines in the native genetic backgrounds grown in simulated parental environments. The foreign CBF2 genotype in the local genetic background reduced long-term mean fitness in Sweden by more than 10%, primarily via effects on survival. In Italy, fitness was reduced by more than 20%, primarily via effects on fecundity. At both sites, the effects were temporally variable and much stronger in some years. The gene-edited lines confirmed that CBF2 encodes the causal variant underlying this genetic trade-off. Additionally, we demonstrated a substantial fitness cost of cold acclimation, which has broad implications for potential maladaptive responses to climate change.

Place, publisher, year, edition, pages
Proceedings of the National Academy of Sciences (PNAS), 2024
Keywords
antagonistic pleiotropy, cold acclimation, genetic trade, local adaptation
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-525515 (URN)10.1073/pnas.2317461121 (DOI)001169138400008 ()38289961 (PubMedID)
Funder
Swedish Research Council, 2016-05435Swedish Research Council, 2020-04434
Available from: 2024-03-26 Created: 2024-03-26 Last updated: 2024-03-26Bibliographically approved
Wunder, J., Fulgione, A., Toräng, P., Wötzel, S., Herzog, M., Obeso, J. R., . . . Coupland, G. (2023). Adaptation of perennial flowering phenology across the European range of Arabis alpina. Proceedings of the Royal Society of London. Biological Sciences, 290(2011), Article ID 20231401.
Open this publication in new window or tab >>Adaptation of perennial flowering phenology across the European range of Arabis alpina
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2023 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 290, no 2011, article id 20231401Article in journal (Refereed) Published
Abstract [en]

Flowering phenology is important in the adaptation of many plants to their local environment, but its adaptive value has not been extensively studied in herbaceous perennials. We used Arabis alpina as a model system to determine the importance of flowering phenology to fitness of a herbaceous perennial with a wide geographical range. Individual plants representative of local genetic diversity (accessions) were collected across Europe, including in Spain, the Alps and Scandinavia. The flowering behaviour of these accessions was documented in controlled conditions, in common-garden experiments at native sites and in situ in natural populations. Accessions from the Alps and Scandinavia varied in whether they required exposure to cold (vernalization) to induce flowering, and in the timing and duration of flowering. By contrast, all Spanish accessions obligately required vernalization and had a short duration of flowering. Using experimental gardens at native sites, we show that an obligate requirement for vernalization increases survival in Spain. Based on our analyses of genetic diversity and flowering behaviour across Europe, we propose that in the model herbaceous perennial A. alpina, an obligate requirement for vernalization, which is correlated with short duration of flowering, is favoured by selection in Spain where the plants experience a long growing season.

Place, publisher, year, edition, pages
Royal Society, 2023
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-519759 (URN)10.1098/rspb.2023.1401 (DOI)001108027100001 ()37989245 (PubMedID)
Funder
German Research Foundation (DFG), TRR 341European Science Foundation (ESF)Swedish Research CouncilGerman Research Foundation (DFG)
Available from: 2024-01-09 Created: 2024-01-09 Last updated: 2024-01-15Bibliographically approved
Petren, H., Thosteman, H., Stift, M., Toräng, P., Ågren, J. & Friberg, M. (2023). Differences in mating system and predicted parental conflict affect post-pollination reproductive isolation in a flowering plant. Evolution, 77(4), 1019-1030
Open this publication in new window or tab >>Differences in mating system and predicted parental conflict affect post-pollination reproductive isolation in a flowering plant
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2023 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 77, no 4, p. 1019-1030Article in journal (Refereed) Published
Abstract [en]

Mating system shifts from outcrossing to selfing are frequent in plant evolution. Relative to outcrossing, selfing is associated with reduced parental conflict over seed provisioning, which may result in postzygotic, asymmetric, reproductive isolation in crosses between populations of different mating systems. To test the hypothesis that post-pollination reproductive isolation between populations increases with increasing differences in mating system and predicted parental conflict, we performed a crossing experiment involving all combinations of three self-compatible populations (with low outcrossing rates), and three self-incompatible populations (with high outcrossing rates) of the arctic-alpine herb Arabis alpina, assessing fitness-related seed and plant traits of the progeny. Predicted levels of parental conflict ("genome strength") were quantified based on strength of self-incompatibility and estimates of outcrossing rates. Crosses between self-compatible and self-incompatible populations yielded very small seeds of low viability, resulting in strong reproductive isolation. In 14 of 15 reciprocal between-population crosses, seeds were heavier when the paternal plant had the stronger genome, and seed mass differences between cross directions increased with an increased difference in parental conflict. Overall, our results suggest that, when sufficiently large, differences in mating system and hence in expected parental conflict may result in strong post-pollination reproductive barriers contributing to speciation.

Place, publisher, year, edition, pages
Oxford University Press (OUP), 2023
Keywords
Arabis alpina, breeding system, mating system, parental conflict, reproductive isolation, speciation
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-508553 (URN)10.1093/evolut/qpad016 (DOI)001010630100008 ()36734045 (PubMedID)
Funder
Swedish Research Council, 2019-04696Carl Tryggers foundation Linnaeus scholarship foundationSwedish Phytogeographical Society
Available from: 2023-08-07 Created: 2023-08-07 Last updated: 2023-08-07
Opedal, Ø. H., Armbruster, W. S., Hansen, T. F., Holstad, A., Pélabon, C., Andersson, S., . . . Bolstad, G. H. (2023). Evolvability and trait function predict phenotypic divergence of plant populations. Proceedings of the National Academy of Sciences of the United States of America, 120(1)
Open this publication in new window or tab >>Evolvability and trait function predict phenotypic divergence of plant populations
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2023 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 120, no 1Article in journal (Refereed) Published
Abstract [en]

Understanding the causes and limits of population divergence in phenotypic traits is a fundamental aim of evolutionary biology, with the potential to yield predictions of adap-tation to environmental change. Reciprocal transplant experiments and the evaluation of optimality models suggest that local adaptation is common but not universal, and some studies suggest that trait divergence is highly constrained by genetic variances and covariances of complex phenotypes. We analyze a large database of population divergence in plants and evaluate whether evolutionary divergence scales positively with standing genetic  variation  within  populations  (evolvability),  as  expected  if  genetic  constraints  are evolutionarily important. We further evaluate differences in divergence and evolva-bility–divergence relationships between reproductive and vegetative traits and between selfing, mixed-mating, and outcrossing species, as these factors are expected to influence both patterns of selection and evolutionary potentials. Evolutionary divergence scaled positively  with  evolvability.  Furthermore,  trait  divergence  was  greater  for  vegetative  traits than for floral (reproductive) traits, but largely independent of the mating system. Jointly, these factors explained ~40% of the variance in evolutionary divergence. The consistency of the evolvability–divergence relationships across diverse species suggests substantial predictability of trait divergence. The results are also consistent with genetic constraints playing a role in evolutionary divergence.

Place, publisher, year, edition, pages
Proceedings of the National Academy of Sciences (PNAS), 2023
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-492669 (URN)10.1073/pnas.2203228120 (DOI)001036961000004 ()36580593 (PubMedID)
Funder
Swedish Research Council, 2021-04777The Crafoord Foundation, 20210661The Research Council of Norway, 287214The Research Council of Norway, 275862
Available from: 2023-01-09 Created: 2023-01-09 Last updated: 2024-01-26Bibliographically approved
Monroe, J. G., Murray, K. D., Xian, W., Srikant, T., Carbonell-Bejerano, P., Becker, C., . . . Weigel, D. (2023). Reply to: Re-evaluating evidence for adaptive mutation rate variation [Letter to the editor]. Nature, 619(7971), E57-E60
Open this publication in new window or tab >>Reply to: Re-evaluating evidence for adaptive mutation rate variation
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2023 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 619, no 7971, p. E57-E60Article in journal, Letter (Refereed) Published
Place, publisher, year, edition, pages
Springer Nature, 2023
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-519730 (URN)10.1038/s41586-023-06315-x (DOI)001122097500013 ()37495874 (PubMedID)
Available from: 2024-01-09 Created: 2024-01-09 Last updated: 2024-03-08Bibliographically approved
Durán, P., Ellis, T. J., Thiergart, T., Ågren, J. & Hacquard, S. (2022). Climate drives rhizosphere microbiome variation and divergent selection between geographically distant Arabidopsis populations. New Phytologist, 236(2), 608-621
Open this publication in new window or tab >>Climate drives rhizosphere microbiome variation and divergent selection between geographically distant Arabidopsis populations
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2022 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 236, no 2, p. 608-621Article in journal (Refereed) Published
Place, publisher, year, edition, pages
John Wiley & SonsWiley, 2022
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-492091 (URN)10.1111/nph.18357 (DOI)000829915700001 ()
Funder
German Research Foundation (DFG)Swedish Research Council, 2016‐05435Swedish Research Council, 2020‐04434
Available from: 2023-01-02 Created: 2023-01-02 Last updated: 2024-01-15Bibliographically approved
Postma, F. M. & Ågren, J. (2022). Effects of primary seed dormancy on lifetime fitness of Arabidopsis thaliana in the field. Annals of Botany, 129(7), 795-808
Open this publication in new window or tab >>Effects of primary seed dormancy on lifetime fitness of Arabidopsis thaliana in the field
2022 (English)In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 129, no 7, p. 795-808Article in journal (Refereed) Published
Abstract [en]

Background and Aims Seed dormancy determines the environmental niche of plants in seasonal environments, and has consequences for plant performance that potentially go far beyond the seed and seedling stages. In this study, we examined the cascading effects of seed dormancy on the expression of subsequent life-history traits and fitness in the annual herb Arabidopsis thaliana. Methods We planted seeds of >200 recombinant inbred lines (RILs) derived from a cross between two locally adapted populations (Italy and Sweden), and both parental genotypes at the native site of the Swedish population in three consecutive years. We quantified the relationship between primary seed dormancy and the expression of subsequent life-history traits and fitness in the RIL population with path analysis. To examine the effects of differences in dormancy on the relative fitness of the two parental genotypes, we planted dormant seeds during the seed dispersal period and non-dormant seeds during the germination period of the local population. Key Results In the RIL population, strong primary dormancy was associated with high seedling survival, but with low adult survival and fecundity, and path analysis indicated that this could be explained by effects on germination timing, rosette size and flowering start. The relationship between primary seed dormancy and germination proportion varied among years, and this was associated with differences in seasonal changes in soil moisture. The planting of dormant and non-dormant seeds indicated that the lower primary dormancy of the local Swedish genotype contributed to its higher germination proportion in two years and to its higher fecundity in one year. Conclusions Our results show that seed dormancy affects trait expression and fitness components across the life cycle, and suggest that among-year variation in the incidence of drought during the germination period should be considered when predicting the consequences of climatic change for population growth and evolution.

Place, publisher, year, edition, pages
Oxford University Press (OUP), 2022
Keywords
Arabidopsis thaliana, germination timing, local adaptation, natural variation, seed dormancy, structural equation modelling (SEM), temporal variation
National Category
Botany
Identifiers
urn:nbn:se:uu:diva-484090 (URN)10.1093/aob/mcac010 (DOI)000763786300001 ()35092679 (PubMedID)
Funder
Swedish Research Council, 2016-05435Swedish Research Council, 2020-04434
Available from: 2022-09-08 Created: 2022-09-08 Last updated: 2022-09-08Bibliographically approved
Monroe, J. G., Srikant, T., Carbonell-Bejerano, P., Becker, C., Lensink, M., Exposito-Alonso, M., . . . Weigel, D. (2022). Mutation bias reflects natural selection in Arabidopsis thaliana. Nature, 602(7895), 101-105
Open this publication in new window or tab >>Mutation bias reflects natural selection in Arabidopsis thaliana
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2022 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 602, no 7895, p. 101-105Article in journal (Refereed) Published
Abstract [en]

Since the first half of the twentieth century, evolutionary theory has been dominated by the idea that mutations occur randomly with respect to their consequences(1). Here we test this assumption with large surveys of de novo mutations in the plant Arabidopsis thaliana. In contrast to expectations, we find that mutations occur less often in functionally constrained regions of the genome-mutation frequency is reduced by half inside gene bodies and by two-thirds in essential genes. With independent genomic mutation datasets, including from the largest Arabidopsis mutation accumulation experiment conducted to date, we demonstrate that epigenomic and physical features explain over 90% of variance in the genome-wide pattern of mutation bias surrounding genes. Observed mutation frequencies around genes in turn accurately predict patterns of genetic polymorphisms in natural Arabidopsis accessions (r = 0.96). That mutation bias is the primary force behind patterns of sequence evolution around genes in natural accessions is supported by analyses of allele frequencies. Finally, we find that genes subject to stronger purifying selection have a lower mutation rate. We conclude that epigenome-associated mutation bias2 reduces the occurrence of deleterious mutations in Arabidopsis, challenging the prevailing paradigm that mutation is a directionless force in evolution.

Place, publisher, year, edition, pages
Springer Nature, 2022
National Category
Genetics Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-473202 (URN)10.1038/s41586-021-04269-6 (DOI)000741978700002 ()35022609 (PubMedID)
Available from: 2022-04-26 Created: 2022-04-26 Last updated: 2023-01-23Bibliographically approved
Zacchello, G., Bomers, S., Böhme, C., Postma, F. & Ågren, J. (2022). Seed dormancy varies widely among Arabidopsis thaliana populations both between and within Fennoscandia and Italy. Ecology and Evolution, 12(3), Article ID e8670.
Open this publication in new window or tab >>Seed dormancy varies widely among Arabidopsis thaliana populations both between and within Fennoscandia and Italy
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2022 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 12, no 3, article id e8670Article in journal (Refereed) Published
Abstract [en]

The timing of germination is a key life-history trait in plants, which is strongly affected by the strength of seed dormancy. Continental-wide variation in seed dormancy has been related to differences in climate and the timing of conditions suitable for seedling establishment. However, for predictions of adaptive potential and consequences of climatic change, information is needed regarding the extent to which seed dormancy varies within climatic regions and the factors driving such variation. We planted 17 Italian and 28 Fennoscandian populations of Arabidopsis thaliana in the greenhouse and at two field sites in Italy and Sweden. To identify possible drivers of among-population variation in seed dormancy, we examined the relationship between seed dormancy and climate at the sites where populations were originally sampled. Seed dormancy was on average stronger in the Italian compared to the Fennoscandian populations, but also varied widely within both regions. Estimates of seed dormancy in the three maternal environments were positively correlated, but seeds had on average stronger dormancy when produced in the greenhouse than at the two field sites. Among Fennoscandian populations, seed dormancy tended to increase with increasing summer temperature and decreasing precipitation at the site of origin. In the smaller sample of Italian populations, no significant association was detected between mean seed dormancy and climate at the site of origin. The correlation between seed dormancy and climatic factors in Fennoscandia suggests that at least some of the among-population variation is adaptive and that climate change will affect selection on this trait. 

Place, publisher, year, edition, pages
John Wiley & SonsWiley, 2022
Keywords
climate change, germination proportion, maternal environmental effect, regional variation, timing of germination
National Category
Ecology
Research subject
Biology with specialization in Ecological Botany
Identifiers
urn:nbn:se:uu:diva-440262 (URN)10.1002/ece3.8670 (DOI)000774963400001 ()35261752 (PubMedID)
Available from: 2021-04-16 Created: 2021-04-16 Last updated: 2024-01-17Bibliographically approved
Petrén, H., Toräng, P., Ågren, J. & Friberg, M. (2021). Evolution of floral scent in relation to self-incompatibility and capacity for autonomous self-pollination in the perennial herb Arabis alpina. Annals of Botany, 127(6), 737-747
Open this publication in new window or tab >>Evolution of floral scent in relation to self-incompatibility and capacity for autonomous self-pollination in the perennial herb Arabis alpina
2021 (English)In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 127, no 6, p. 737-747Article in journal (Refereed) Published
Abstract [en]

Background and Aims

The transition from outcrossing to selfing is a frequent evolutionary shift in flowering plants and is predicted to result in reduced allocation to pollinator attraction if plants can self-pollinate autonomously. The evolution of selfing is associated with reduced visual floral signalling in many systems, but effects on floral scent have received less attention. We compared multiple populations of the arctic–alpine herb Arabis alpina (Brassicaceae), and asked whether the transition from self-incompatibility to self-compatibility has been associated with reduced visual and chemical floral signalling. We further examined whether floral signalling differ between self-compatible populations with low and high capacity for autonomous self-pollination, as would be expected if benefits of signalling decrease with reduced dependence on pollinators for pollen transfer.

Methods

In a common garden we documented flower size and floral scent emission rate and composition in eight self-compatible and nine self-incompatible A. alpina populations. These included self-compatible Scandinavian populations with high capacity for autonomous self-pollination, self-compatible populations with low capacity for autonomous self-pollination from France and Spain, and self-incompatible populations from Italy and Greece.

Key Results

The self-compatible populations produced smaller and less scented flowers than the self-incompatible populations. However, flower size and scent emission rate did not differ between self-compatible populations with high and low capacity for autonomous self-pollination. Floral scent composition differed between self-compatible and self-incompatible populations, but also varied substantially among populations within the two categories.

Conclusions

Our study demonstrates extensive variation in floral scent among populations of a geographically widespread species. Contrary to expectation, floral signalling did not differ between self-compatible populations with high and low capacity for autonomous self-pollination, indicating that dependence on pollinator attraction can only partly explain variation in floral signalling. Additional variation may reflect adaptation to other aspects of local environments, genetic drift, or a combination of these processes.

Place, publisher, year, edition, pages
Oxford University Press, 2021
Keywords
Arabis alpina, floral scent, intraspecific variation, mating system, self-incompatibility, selfing syndrome, volatile organic compound (VOC)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-448803 (URN)10.1093/aob/mcab007 (DOI)000661515800005 ()33555338 (PubMedID)
Funder
Swedish Research CouncilCarl Tryggers foundation
Available from: 2021-07-09 Created: 2021-07-09 Last updated: 2024-01-15Bibliographically approved
Projects
Ecology and evolution of plant adaptation [2009-05396_VR]; Uppsala University24th Annual Meeting of the Scandinavian Association for Pollination Ecology (SCAPE) [2010-05967_VR]; Uppsala UniversitySvensk finansiering av projekt i ESFs Eurocores A.alpina perenniali (09-EuroEEFG-FP-018 Jon Ågren) [2010-07534_VR]; Uppsala UniversityEcology and evolution of plant adaptation [2012-04009_VR]; Uppsala UniversitySCAPE 2016 ‚Äì 30th Annual Meeting of the Scandinavian Association for Pollination Ecology, Abisko, Sweden 13-16 October 2016 [2016-00576_VR]; Uppsala UniversityAdaptiv populationsdifferentiering hos växter [2016-05435_VR]; Uppsala University; Publications
Lee, G., Sanderson, B. J., Ellis, T. J., Dilkes, B. P., McKay, J. K., Ågren, J. & Oakley, C. G. (2024). A large-effect fitness trade-off across environments is explained by a single mutation affecting cold acclimation. Proceedings of the National Academy of Sciences of the United States of America, 121(6), Article ID e2317461121.
Adaptiv populationsdifferentiering hos växter [2020-04434_VR]; Uppsala University; Publications
Lee, G., Sanderson, B. J., Ellis, T. J., Dilkes, B. P., McKay, J. K., Ågren, J. & Oakley, C. G. (2024). A large-effect fitness trade-off across environments is explained by a single mutation affecting cold acclimation. Proceedings of the National Academy of Sciences of the United States of America, 121(6), Article ID e2317461121.
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ORCID iD: ORCID iD iconorcid.org/0000-0001-9573-2463

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