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Postma, F. M. & Ågren, J. (2018). Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana. Molecular Ecology, 27(11), 2498-2511
Open this publication in new window or tab >>Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana
2018 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 11, p. 2498-2511Article in journal (Refereed) Published
Abstract [en]

Incomplete information regarding both selection regimes and the genetic basis of fitness limits our understanding of adaptive evolution. Among-year variation in the genetic basis of fitness is rarely quantified, and estimates of selection are typically based on single components of fitness, thus potentially missing conflicting selection acting during other life-history stages. Here, we examined among-year variation in selection on a key life-history trait and the genetic basis of fitness covering the whole life cycle in the annual plant Arabidopsis thaliana. We planted freshly matured 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 selection against the nonlocal Italian genotype, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on timing of germination during different life stages. In all 3years, the local Swedish genotype outperformed the nonlocal Italian genotype. However, both the contribution of early life stages to relative fitness, and the effects of fitness QTL varied among years. Timing of germination was under conflicting selection through seedling establishment vs. adult survival and fecundity, and both the direction and magnitude of net selection varied among years. Our results demonstrate that selection during early life stages and the genetic basis of fitness can vary markedly among years, emphasizing the need for multiyear studies considering the whole life cycle for a full understanding of natural selection and mechanisms maintaining local adaptation.

Place, publisher, year, edition, pages
John Wiley & Sons, 2018
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-302861 (URN)10.1111/mec.14697 (DOI)000434152100002 ()29676059 (PubMedID)
Funder
Swedish Research Council, 2016-05435
Available from: 2016-09-12 Created: 2016-09-12 Last updated: 2018-08-31Bibliographically approved
Price, N., Moyers, B. T., Lopez, L., Lasky, J. R., Monroe, J. G., Mullen, J. L., . . . McKay, J. K. (2018). Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 115(19), 5028-5033
Open this publication in new window or tab >>Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana
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2018 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 115, no 19, p. 5028-5033Article in journal (Refereed) Published
Abstract [en]

Evidence for adaptation to different climates in the model species Arabidopsis thaliana is seen in reciprocal transplant experiments, but the genetic basis of this adaptation remains poorly understood. Field-based quantitative trait locus (QTL) studies provide direct but low-resolution evidence for the genetic basis of local adaptation. Using high-resolution population genomic approaches, we examine local adaptation along previously identified genetic trade-off (GT) and conditionally neutral (CN) QTLs for fitness between locally adapted Italian and Swedish A. thaliana populations [angstrom gren J, et al. (2013) Proc Natl Acad Sci USA 110: 21077-21082]. We find that genomic regions enriched in high F-ST SNPs colocalize with GT QTL peaks. Many of these high F-ST regions also colocalize with regions enriched for SNPs significantly correlated to climate in Eurasia and evidence of recent selective sweeps in Sweden. Examining unfolded site frequency spectra across genes containing high F-ST SNPs suggests GTs may be due to more recent adaptation in Sweden than Italy. Finally, we collapse a list of thousands of genes spanning GT QTLs to 42 genes that likely underlie the observed GTs and explore potential biological processes driving these trade-offs, from protein phosphorylation, to seed dormancy and longevity. Our analyses link population genomic analyses and field-based QTL studies of local adaptation, and emphasize that GTs play an important role in the process of local adaptation.

Place, publisher, year, edition, pages
NATL ACAD SCIENCES, 2018
Keywords
divergent selection, ecotype, FST, selective sweep, tradeoff
National Category
Genetics Ecology
Identifiers
urn:nbn:se:uu:diva-356386 (URN)10.1073/pnas.1719998115 (DOI)000431639100071 ()29686078 (PubMedID)
Funder
Swedish Research CouncilNIH (National Institute of Health), R01GM078204
Available from: 2018-08-15 Created: 2018-08-15 Last updated: 2018-08-15Bibliographically approved
Laenen, B., Tedder, A., Nowak, M. D., Toräng, P., Wunder, J., Wötzel, S., . . . Slotte, T. (2018). Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina. Proceedings of the National Academy of Sciences of the United States of America, 115(4), 816-821
Open this publication in new window or tab >>Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina
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2018 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 115, no 4, p. 816-821Article in journal (Refereed) Published
Abstract [en]

Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.

Place, publisher, year, edition, pages
NATL ACAD SCIENCES, 2018
Keywords
self-fertilization, demographic history, bottleneck, fitness effects, genetic load
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-343798 (URN)10.1073/pnas.1707492115 (DOI)000423097800070 ()29301967 (PubMedID)
Funder
Swedish National Infrastructure for Computing (SNIC), snic2014-1-194, b2013022, b2013237Swedish Research CouncilScience for Life Laboratory - a national resource center for high-throughput molecular bioscience
Available from: 2018-03-05 Created: 2018-03-05 Last updated: 2018-03-05Bibliographically approved
Chapurlat, E., Anderson, J., Ågren, J., Friberg, M. & Sletvold, N. (2018). Diel pattern of floral scent emission matches the relative importance of diurnal and nocturnal pollinators in populations of Gymnadenia conopsea. Annals of Botany, 121, 711-721
Open this publication in new window or tab >>Diel pattern of floral scent emission matches the relative importance of diurnal and nocturnal pollinators in populations of Gymnadenia conopsea
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2018 (English)In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 121, p. 711-721Article in journal (Refereed) Published
Abstract [en]

Background and Aims

Floral scent is considered an integral component of pollination syndromes, and its composition and timing of emission are thus expected to match the main pollinator type and time of activity. While floral scent differences among plant species with different pollination systems can be striking, studies on intraspecific variation are sparse, which limits our understanding of the role of pollinators in driving scent divergence.

Methods

Here, we used dynamic headspace sampling to quantify floral scent emission and composition during the day and at night in the natural habitat of six Scandinavian populations of the fragrant orchid Gymnadenia conopsea. We tested whether diel scent emission and composition match pollinator type by comparing four populations in southern Sweden, where nocturnal pollinators are more important for plant reproductive success than are diurnal pollinators, with two populations in central Norway, where the opposite is true. To determine to what extent scent patterns quantified in the field reflected plasticity, we also measured scent emission in a common growth chamber environment.

Key Results

Both scent composition and emission rates differed markedly between day and night, but only the latter varied significantly among populations. The increase in scent emission rate at night was considerably stronger in the Swedish populations compared with the Norwegian populations. These patterns persisted when plants were transferred to a common environment, suggesting a genetic underpinning of the scent variation.

Conclusions

The results are consistent with a scenario where spatial variation in relative importance of nocturnal and diurnal pollinators has resulted in selection for different scent emission rhythms. Our study highlights the importance of adding a characterization of diel variation of scent emission rates to comparative studies of floral scent, which so far have often focused on scent composition only.

Keywords
diel variation, diurnal and nocturnal pollination, floral evolution, floral scent, geographic variation, Gymnadenia conopsea (fragrant orchid), plasticity, population differentiation, scent emission rate, scent rhythm, semi-generalkized pollination, spatial variation
National Category
Evolutionary Biology Ecology
Identifiers
urn:nbn:se:uu:diva-358243 (URN)10.1093/aob/mcx203 (DOI)
Available from: 2018-08-26 Created: 2018-08-26 Last updated: 2018-08-27Bibliographically approved
Urbina, H., Breed, M. F., Zhao, W., Gurrala, K. L., Andersson, S. G. .., Ågren, J., . . . Rosling, A. (2018). Specificity in Arabidopsis thaliana recruitment of root fungal communities from soil and rhizosphere. Fungal Biology, 122(4), 231-240
Open this publication in new window or tab >>Specificity in Arabidopsis thaliana recruitment of root fungal communities from soil and rhizosphere
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2018 (English)In: Fungal Biology, ISSN 1878-6146, E-ISSN 1878-6162, Vol. 122, no 4, p. 231-240Article in journal (Refereed) Published
Abstract [en]

Biotic and abiotic conditions in soil pose major constraints on growth and reproductive success of plants. Fungi are important agents in plant soil interactions but the belowground mycobiota associated with plants remains poorly understood. We grew one genotype each from Sweden and Italy of the widely studied plant model Arabidopsis thaliana. Plants were grown under controlled conditions in organic topsoil local to the Swedish genotype, and harvested after ten weeks. Total DNA was extracted from three belowground compartments: endosphere (sonicated roots), rhizosphere and bulk soil, and fungal communities were characterized from each by amplification and sequencing of the fungal barcode region ITS2. Fungal species diversity was found to decrease from bulk soil to rhizosphere to endo-sphere. A significant effect of plant genotype on fungal community composition was detected only in the endosphere compartment. Despite A. thaliana being a non-mycorrhizal plant, it hosts a number of known mycorrhiza fungi in its endosphere compartment, which is also colonized by endophytic, pathogenic and saprotrophic fungi. Species in the Archaeorhizomycetes were most abundant in rhizosphere samples suggesting an adaptation to environments with high nutrient turnover for some of these species. We conclude that A. thaliana endosphere fungal communities represent a selected subset of fungi recruited from soil and that plant genotype has small but significant quantitative and qualitative effects on these communities.

Keywords
Arabidopsis, Archaeorhizomcyetes, Brassicaceae, Ion Torrent, ITS metabarcoding, Rhizosphere
National Category
Botany
Identifiers
urn:nbn:se:uu:diva-354246 (URN)10.1016/j.funbio.2017.12.013 (DOI)000430773300005 ()29551197 (PubMedID)
Funder
Swedish Research Council, 349-2007-8731Swedish Research Council, 2012-3950Australian Research Council, DE150100542Australian Research Council, DP150103414
Note

De 2 första författarna delar förstaförfattarskapet.

Available from: 2018-06-19 Created: 2018-06-19 Last updated: 2018-06-19Bibliographically approved
Ågren, J., Oakley, C. G., Lundemo, S. & Schemske, D. W. (2017). Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping. Evolution, 71(3), 550-564
Open this publication in new window or tab >>Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping
2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 3, p. 550-564Article in journal (Refereed) Published
Abstract [en]

To identify the ecological and genetic mechanisms of local adaptation requires estimating selection on traits, identifying their genetic basis, and evaluating whether divergence in adaptive traits is due to conditional neutrality or genetic trade-offs. To this end, we conducted field experiments for three years using recombinant inbred lines (RILs) derived from two ecotypes of Arabidopsis thaliana (Italy, Sweden), and at each parental site examined selection on flowering time and mapped quantitative trait loci (QTL). There was strong selection for early flowering in Italy, but weak selection in Sweden. Eleven distinct flowering time QTL were detected, and for each the Italian genotype caused earlier flowering. Twenty-seven candidate genes were identified, two of which (FLC and VIN3) appear under major flowering time QTL in Italy. Seven of eight QTL in Italy with narrow credible intervals colocalized with previously reported fitness QTL, in comparison to three of four in Sweden. The results demonstrate that the magnitude of selection on flowering time differs strikingly between our study populations, that the genetic basis of flowering time variation is multigenic with some QTL of large effect, and suggest that divergence in flowering time between ecotypes is due mainly to conditional neutrality.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
Adaptation, Arabidopsis thaliana, phenology, recombinant inbred lines, selection, trade-off
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-320840 (URN)10.1111/evo.13126 (DOI)000396039000004 ()27859214 (PubMedID)
Funder
Swedish Research Council
Available from: 2017-04-26 Created: 2017-04-26 Last updated: 2017-04-26Bibliographically approved
Toräng, P., Vikström, L., Wunder, J., Wötzel, S., Coupland, G. & Ågren, J. (2017). Evolution of the selfing syndrome: Anther orientation and herkogamy together determine reproductive assurance in a self-compatible plant. Evolution, 71(9), 2206-2218
Open this publication in new window or tab >>Evolution of the selfing syndrome: Anther orientation and herkogamy together determine reproductive assurance in a self-compatible plant
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2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 9, p. 2206-2218Article in journal (Refereed) Published
Abstract [en]

Capacity for autonomous self-fertilization provides reproductive assurance, has evolved repeatedly in the plant kingdom, and typically involves several changes in flower morphology and development (the selfing syndrome). Yet, the relative importance of different traits and trait combinations for efficient selfing and reproductive success in pollinator-poor environments is poorly known. In a series of experiments, we tested the importance of anther-stigma distance and the less studied trait anther orientation for efficiency of selfing in the perennial herb Arabis alpina. Variation in flower morphology among eight self-compatible European populations was correlated with efficiency of self-pollination and with pollen limitation in a common-garden experiment. To examine whether anther-stigma distance and anther orientation are subject to directional and/or correlational selection, and whether this is because these traits affect pollination success, we planted a segregating F2 population at two native field sites. Selection strongly favored a combination of introrse anthers and reduced anther-stigma distance at a site where pollinator activity was low, and supplemental hand-pollination demonstrated that this was largely because of their effect on securing self-pollination. The results suggest that concurrent shifts in more than one trait can be crucial for the evolution of efficient self-pollination and reproductive assurance in pollinator-poor habitats.

Place, publisher, year, edition, pages
John Wiley & Sons, 2017
Keywords
Adaptive evolution, floral morphology, mating system, natural selection, pollination
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-335645 (URN)10.1111/evo.13308 (DOI)000409486000005 ()28722132 (PubMedID)
Available from: 2017-12-11 Created: 2017-12-11 Last updated: 2017-12-11Bibliographically approved
Trunschke, J., Sletvold, N. & Ågren, J. (2017). Interaction intensity and pollinator-mediated selection. New Phytologist, 214(3), 1381-1389
Open this publication in new window or tab >>Interaction intensity and pollinator-mediated selection
2017 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 214, no 3, p. 1381-1389Article in journal (Refereed) Published
Abstract [en]

In animal-pollinated plants, the opportunity for selection and the strength of pollinatormediated selection are expected to increase with the degree of pollen limitation. However, whether differences in pollen limitation can explain variation in pollinator-mediated and net selection among animal-pollinated species is poorly understood. In the present study, we quantified pollen limitation, variance in relative fitness and pollinator- mediated selection on five traits important for pollinator attraction (flowering start, plant height, flower number, flower size) and pollination efficiency (spur length) in natural populations of 12 orchid species. Pollinator-mediated selection was quantified by subtracting estimates of selection gradients for plants receiving supplemental hand-pollination from estimates obtained for open-pollinated control plants. Mean pollen limitation ranged from zero to 0.96. Opportunity for selection, pollinatormediated selection and net selection were all positively related to pollen limitation, whereas nonpollinator-mediated selection was not. Opportunity for selection varied five-fold, strength of pollinator-mediated selection varied three-fold and net selection varied 1.5-fold among species. Supplemental hand-pollination reduced both opportunity for selection and selection on floral traits. The results show that the intensity of biotic interactions is an important determinant of the selection regime, and indicate that the potential for pollinator-mediated selection and divergence in floral traits is particularly high in species that are strongly pollen-limited.

Keywords
biotic interactions, natural selection, opportunity for selection, Orchidaceae, pollen limitation, pollinator-mediated selection
National Category
Evolutionary Biology Ecology
Identifiers
urn:nbn:se:uu:diva-326362 (URN)10.1111/nph.14479 (DOI)000402403900041 ()28240377 (PubMedID)
Funder
Swedish Research CouncilSwedish Research Council Formas
Available from: 2017-07-10 Created: 2017-07-10 Last updated: 2018-04-24Bibliographically approved
Colautti, R. I., Ågren, J. & Anderson, J. T. (2017). Phenological shifts of native and invasive species under climate change: insights from the Boechera - Lythrum model. Philosophical Transactions of the Royal Society of London. Biological Sciences, 372(1712), Article ID 20160032.
Open this publication in new window or tab >>Phenological shifts of native and invasive species under climate change: insights from the Boechera - Lythrum model
2017 (English)In: Philosophical Transactions of the Royal Society of London. Biological Sciences, ISSN 0962-8436, E-ISSN 1471-2970, Vol. 372, no 1712, article id 20160032Article, review/survey (Refereed) Published
Abstract [en]

Warmer and drier climates have shifted phenologies of many species. However, the magnitude and direction of phenological shifts vary widely among taxa, and it is often unclear when shifts are adaptive or how they affect long-term viability. Here, we model evolution of flowering phenology based on our long-term research of two species exhibiting opposite shifts in floral phenology: Lythrum salicaria, which is invasive in North America, and the sparse Rocky Mountain native Boechera stricta. Genetic constraints are similar in both species, but differences in the timing of environmental conditions that favour growth lead to opposite phenological shifts under climate change. As temperatures increase, selection is predicted to favour earlier flowering in native B. stricta while reducing population viability, even if populations adapt rapidly to changing environmental conditions. By contrast, warming is predicted to favour delayed flowering in both native and introduced L. salicaria populations while increasing long-term viability. Relaxed selection from natural enemies in invasive L. salicaria is predicted to have little effect on flowering time but a large effect on reproductive fitness. Our approach highlights the importance of understanding ecological and genetic constraints to predict the ecological consequences of evolutionary responses to climate change on contemporary timescales. This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.

Keywords
growth rate, flowering time, optimal control theory, Boechera stricta, Lythrum salicaria
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-314800 (URN)10.1098/rstb.2016.0032 (DOI)000390321500005 ()
Funder
Swedish Research Council
Available from: 2017-02-07 Created: 2017-02-06 Last updated: 2017-11-29Bibliographically approved
Sletvold, N., Tye, M. R. & Ågren, J. (2017). Resource- and pollinator-mediated selection on floral traits. Functional Ecology, 31(1), 135-141
Open this publication in new window or tab >>Resource- and pollinator-mediated selection on floral traits
2017 (English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 31, no 1, p. 135-141Article in journal (Refereed) Published
Abstract [en]

1. Female reproductive success is predicted to be simultaneously limited by the availability of pollen and resources. Selection on floral traits results from both factors, but their relative importance and interaction is poorly understood. 2. We increased nutrient and pollen availability of the orchid Dactylorhiza lapponica in a factorial experiment to quantify resource-and pollinator-mediated selection on floral traits. Hand-pollination increased female fitness (number of fruits 9 mean fruit mass) by 74% in both nutrient treatments, whereas nutrient addition did not significantly affect female fitness. 3. There was selection for more flowers and longer spurs, and selection on spur length was significantly pollinator-mediated and of similar strength across nutrient treatments (Delta beta(poll) = 0.54 and Delta beta(poll_NPK) = 0.59). There was no statistically significant resource-mediated selection. Nutrient addition increased flower size the following year, but did not affect flower or fruit production, or selection on any trait. 4. The results demonstrate that D. lapponica does not increase flower production in response to nutrient addition, that the increase in female fitness in response to hand-pollination is not resource limited, and suggest that natural resource variation does not influence selection on floral traits. The study illustrates that crossed manipulations of pollen and resources can clarify their relative importance for selection on floral traits.

Place, publisher, year, edition, pages
WILEY-BLACKWELL, 2017
Keywords
biotic interactions, floral display, hand-pollination, natural selection, nutrient-addition, pollen limitation, resource limitation
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-319811 (URN)10.1111/1365-2435.12757 (DOI)000394372700015 ()
Funder
Swedish Research Council Formas
Available from: 2017-04-10 Created: 2017-04-10 Last updated: 2018-08-14Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0001-9573-2463

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