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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
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: 2017-11-29Bibliographically approved
Postma, F. M. & Ågren, J. (2016). Early life stages contribute strongly to local adaptation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 113(27), 7590-7595
Open this publication in new window or tab >>Early life stages contribute strongly to local adaptation in Arabidopsis thaliana
2016 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 113, no 27, p. 7590-7595Article in journal (Refereed) Published
Abstract [en]

The magnitude and genetic basis of local adaptation is of fundamental interest in evolutionary biology. However, field experiments usually do not consider early life stages, and therefore may underestimate local adaptation and miss genetically based tradeoffs. We examined the contribution of differences in seedling establishment to adaptive differentiation and the genetic architecture of local adaptation using recombinant inbred lines (RIL) derived from a cross between two locally adapted populations (Italy and Sweden) of the annual plant Arabidopsis thaliana. We planted freshly matured, dormant seeds (> 180 000) representing >200 RILs at the native field sites of the parental genotypes, estimated the strength of selection during different life stages, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on seed dormancy. We found that selection during the seedling establishment phase contributed strongly to the fitness advantage of the local genotype at both sites. With one exception, local alleles of the eight distinct establishment QTL were favored. The major QTL for establishment and total fitness showed evidence of a fitness tradeoff and was located in the same region as the major seed dormancy QTL and the dormancy gene DELAY OF GERMINATION 1 (DOG1). RIL seed dormancy could explain variation in seedling establishment and fitness across the life cycle. Our results demonstrate that genetically based differences in traits affecting performance during early life stages can contribute strongly to adaptive differentiation and genetic tradeoffs, and should be considered for a full understanding of the ecology and genetics of local adaptation.

Keywords
adaptive differentiation, divergent selection, genetic tradeoff, pleiotropy, QTL mapping
National Category
Botany Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-300043 (URN)10.1073/pnas.1606303113 (DOI)000379021700079 ()27330113 (PubMedID)
Available from: 2016-08-02 Created: 2016-08-02 Last updated: 2017-11-28Bibliographically approved
Lehndal, L., Hambäck, P., Ericson, L. & Ågren, J. (2016). Herbivory strongly influences among-population variation in reproductive output of Lythrum salicaria in its native range. Oecologia, 180(4), 1159-1171
Open this publication in new window or tab >>Herbivory strongly influences among-population variation in reproductive output of Lythrum salicaria in its native range
2016 (English)In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 180, no 4, p. 1159-1171Article in journal (Refereed) Published
Abstract [en]

Herbivory can negatively affect several components of plant reproduction. Yet, because of a lack of experimental studies involving multiple populations, the extent to which differences in herbivory contribute to among-population variation in plant reproductive success is poorly known. We determined experimentally the effects of insect herbivory on reproductive output in nine natural populations of the perennial herb Lythrum salicaria along a disturbance gradient in an archipelago in northern Sweden, and we quantified among-population differentiation in resistance to herbivory in a common-garden experiment in the same area. The intensity of leaf herbivory varied >500-fold and mean female reproductive success >400-fold among the study populations. The intensity of herbivory was lowest in populations subject to strong disturbance from ice and wave action. Experimental removal of insect herbivores showed that the effect of herbivory on female reproductive success was correlated with the intensity of herbivory and that differences in insect herbivory could explain much of among-population variation in the proportion of plants flowering and seed production. Population differentiation in resistance to herbivory was limited. The results demonstrate that the intensity of herbivory is a major determinant of flowering and seed output in L. salicaria, but that differences in herbivory are not associated with differences in plant resistance at the spatial scale examined. They further suggest that the physical disturbance regime may strongly influence the performance and abundance of perennial herbs not only because of its effect on interspecific competition, but also because of effects on interactions with specialized herbivores.

Keywords
Disturbance gradient, Flowering, Plant-herbivore interactions, Plant resistance, Seed production
National Category
Natural Sciences
Research subject
Biology with specialization in Ecological Botany
Identifiers
urn:nbn:se:uu:diva-247086 (URN)10.1007/s00442-015-3520-2 (DOI)000373186100022 ()26678991 (PubMedID)
Funder
Swedish Research Council
Note

Erratum in: OECOLOGIA 180(4), pg. 1173-1174. DOI: 10.1007/s00442-016-3570-0

Available from: 2015-03-13 Created: 2015-03-13 Last updated: 2017-12-04Bibliographically approved
Postma, F. M., Lundemo, S. & Ågren, J. (2016). Seed dormancy cycling and mortality differ between two locally adapted populations of Arabidopsis thaliana. Annals of Botany, 117(2), 249-256
Open this publication in new window or tab >>Seed dormancy cycling and mortality differ between two locally adapted populations of Arabidopsis thaliana
2016 (English)In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 117, no 2, p. 249-256Article in journal (Refereed) Published
Abstract [en]

Background and Aims Intraspecific variation in seed bank dynamics should contribute to local adaptation, but is not well studied. The extent to which genetic and environmental factors affect dormancy cycling and seed mortality was investigated in the annual herb Arabidopsis thaliana by conducting a reciprocal seed burial experiment. Methods Seeds from two locally adapted populations (from Italy and Sweden) were buried at both of the sites of origin, and seed mortality and germinability were determined during the following 2 years for initially non-dormant glasshouse-matured seeds and dormant field-matured seeds. Key Results Mean soil temperature was higher at the Italian site compared with the Swedish site throughout the year, and the germination proportions were in general higher for seeds buried in Italy than in Sweden. The rate of secondary dormancy induction of the Italian genotype was faster than that of the Swedish genotype at both sites, while the opposite was true for the rate of dormancy release, at least at the Swedish site. The comparison of nondormant glasshouse seeds with dormant field seeds demonstrated that A. thaliana seeds can adjust their dormancy levels to current environmental conditions, and suggests that maternal environmental conditions have only minor effects on dormancy cycles. At both sites, locally produced seeds had low germinability in the first year compared with the second year, suggesting that a considerable fraction of the seeds would enter the seed bank. In Italy, but not in Sweden, seed mortality increased rapidly during the second year of burial. Conclusions This is the first demonstration of intraspecific genetic differentiation in the annual seed dormancy cycle of any species, and the documented difference is likely to contribute to local adaptation. The results suggest that the contribution of a seed bank to seedling recruitment should vary among environments due to differences in the rate of seed mortality.

Keywords
Arabidopsis thaliana, bet-hedging, dormancy cycling, local adaptation, natural variation, physiological dormancy, secondary dormancy, seed bank, seed mortality, seed predation
National Category
Botany
Identifiers
urn:nbn:se:uu:diva-281828 (URN)10.1093/aob/mcv171 (DOI)000370194800003 ()26637384 (PubMedID)
Funder
Swedish Research Council
Available from: 2016-04-06 Created: 2016-03-30 Last updated: 2017-11-30Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0001-9573-2463

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