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  • 1.
    Akiyama, Reiko
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Conflicting selection on the timing of germination in a natural population of Arabidopsis thaliana2014In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 27, no 1, p. 193-199Article in journal (Refereed)
    Abstract [en]

    The timing of germination is a key life-history trait that may strongly influence plant fitness and that sets the stage for selection on traits expressed later in the life cycle. In seasonal environments, the period favourable for germination and the total length of the growing season are limited. The optimal timing of germination may therefore be governed by conflicting selection through survival and fecundity. We conducted a field experiment to examine the effects of timing of germination on survival, fecundity and overall fitness in a natural population of the annual herb Arabidopsis thaliana in north-central Sweden. Seedlings were transplanted at three different times in late summer and in autumn covering the period of seed germination in the study population. Early germination was associated with low seedling survival, but also with high survival and fecundity among established plants. The advantages of germinating early more than balanced the disadvantage and selection favoured early germination. The results suggest that low survival among early germinating seeds is the main force opposing the evolution of earlier germination and that the optimal timing of germination should vary in space and time as a function of the direction and strength of selection acting during different life-history stages.

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    Akiyama & Ågren JEB 2014
  • 2.
    Akiyama, Reiko
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Magnitude and timing of leaf damage affect seed production in a natural population of Arabidopsis thaliana (Brassicaceae)2012In: PLOS ONE, E-ISSN 1932-6203, Vol. 7, no 1, p. e30015-Article in journal (Refereed)
    Abstract [en]

    Background: The effect of herbivory on plant fitness varies widely. Understanding the causes of this variation is of considerable interest because of its implications for plant population dynamics and trait evolution. We experimentally defoliated the annual herb Arabidopsis thaliana in a natural population in Sweden to test the hypotheses that (a) plant fitness decreases with increasing damage, (b) tolerance to defoliation is lower before flowering than during flowering, and (c) defoliation before flowering reduces number of seeds more strongly than defoliation during flowering, but the opposite is true for effects on seed size.

    Methodology/Principal Findings: In a first experiment, between 0 and 75% of the leaf area was removed in May from plants that flowered or were about to start flowering. In a second experiment, 0, 25%, or 50% of the leaf area was removed from plants on one of two occasions, in mid April when plants were either in the vegetative rosette or bolting stage, or in mid May when plants were flowering. In the first experiment, seed production was negatively related to leaf area removed, and at the highest damage level, also mean seed size was reduced. In the second experiment, removal of 50% of the leaf area reduced seed production by 60% among plants defoliated early in the season at the vegetative rosettes, and by 22% among plants defoliated early in the season at the bolting stage, but did not reduce seed output of plants defoliated one month later. No seasonal shift in the effect of defoliation on seed size was detected.

    Conclusions/Significance: The results show that leaf damage may reduce the fitness of A. thaliana, and suggest that in this population leaf herbivores feeding on plants before flowering should exert stronger selection on defence traits than those feeding on plants during flowering, given similar damage levels.

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  • 3.
    Angert, Amy L.
    et al.
    Univ British Columbia, Dept Bot & Zool, Vancouver, BC V6T 1Z4, Canada..
    Bontrager, Megan G.
    Univ Calif Davis, Dept Ecol & Evolut, Davis, CA 95616 USA..
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    What Do We Really Know About Adaptation at Range Edges?2020In: ANNUAL REVIEW OF ECOLOGY, EVOLUTION, AND SYSTEMATICS, VOL 51, 2020 / [ed] Futuyma, D J, PALO ALTO USA: ANNUAL REVIEWS, 2020, p. 341-361Chapter in book (Refereed)
    Abstract [en]

    Recent theory and empirical evidence have provided new insights regarding how evolutionary forces interact to shape adaptation at stable and transient range margins. Predictions regarding trait divergence at leading edges are frequently supported. However, declines in fitness at and beyond edges show that trait divergence has sometimes been insufficient to maintain high fitness, so identifying constraints to adaptation at range edges remains a key challenge. Indirect evidence suggests that range expansion may be limited by adaptive genetic variation, but direct estimates of genetic constraints at and beyond range edges are still scarce. Sequence data suggest increased genetic load in edge populations in several systems, but its causes and fitness consequences are usually poorly understood. The balance between maladaptive and positive effects of gene flow on fitness at range edges deserves further study. It is becoming increasingly clear that characterizations about degree of adaptation based solely on geographical peripherality are unsupported.

  • 4.
    Boberg, Elin
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Alexandersson, Ronny
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Jonsson, Magdalena
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Maad, Johanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Nilsson, Anders L.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Pollinator shifts and the evolution of spur length in the moth-pollinated orchid Platanthera bifolia2014In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 113, no 2, p. 267-275Article in journal (Refereed)
    Abstract [en]

    Plantpollinator interactions are thought to have shaped much of floral evolution. Yet the relative importance of pollinator shifts and coevolutionary interactions for among-population variation in floral traits in animal-pollinated species is poorly known. This study examined the adaptive significance of spur length in the moth-pollinated orchid Platanthera bifolia. Geographical variation in the length of the floral spur of P. bifolia was documented in relation to variation in the pollinator fauna across Scandinavia, and a reciprocal translocation experiment was conducted in south-east Sweden between a long-spurred woodland population and a short-spurred grassland population. Spur length and pollinator fauna varied among regions and habitats, and spur length was positively correlated with the proboscis length of local pollinators. In the reciprocal translocation experiment, long-spurred woodland plants had higher pollination success than short-spurred grassland plants at the woodland site, while no significant difference was observed at the grassland site. The results are consistent with the hypothesis that optimal floral phenotype varies with the morphology of the local pollinators, and that the evolution of spur length in P. bifolia has been largely driven by pollinator shifts.

  • 5.
    Boberg, Elin
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Despite their apparent integration, spur length but not perianth size affects reproductive success in the moth-pollinated orchid Platanthera bifolia2009In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 23, no 5, p. 1022-1028Article in journal (Refereed)
    Abstract [en]

    The evolution of many floral traits is thought to have been shaped  by pollinator-mediated selection for increased attractiveness or an   improved mechanical fit of flowers to pollinators. Yet, few studies have examined experimentally the independent and interactive effects of   different aspects of flower morphology on plant reproductive success.   In the orchid Platanthera bifolia, perianth size and spur length are   positively correlated within and among populations. To test the hypothesis that pollination success and seed output increases with   increasing perianth size and spur length, we manipulated the two traits   in a factorial design in a long-spurred population of P. bifolia   pollinated by long-tongued hawkmoths. Additionally, to determine   whether differences in selfing rate can explain variation in fruit set   and fruit size, we performed controlled self- and cross-pollination.   Plants with long spurs had more flowers pollinated, more pollen removed   and produced more and larger fruits compared to plants with short   spurs. In contrast, perianth size did not affect the pollination   success or fruit production of P. bifolia.   Fruit production and fruit size did not differ among flowers pollinated   with self- and cross pollen, respectively. This indicates that reduced   pollen deposition rather than pollinator-mediated self-pollination   caused the reduction in fruit set and fruit volume observed after   shortening of the spur.   The results demonstrate that spur length, but not perianth size, is   critical for reproductive success in P. bifolia, and suggest that   among-population differentiation in perianth size may reflect a  correlated response to selection on spur length. The results are  consistent with the hypothesis that visual display is less important   than other cues for the reproductive success of P. bifolia, and   underscore the necessity to experimentally examine the functional   significance of putatively adaptive traits.

  • 6.
    Chapurlat, Elodie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Anderson, Joseph
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Friberg, Magne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Sletvold, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Diel pattern of floral scent emission matches the relative importance of diurnal and nocturnal pollinators in populations of Gymnadenia conopsea2018In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 121, p. 711-721Article in journal (Refereed)
    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.

  • 7.
    Chapurlat, Elodie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Le Roncé, Iris
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Master BioSciences, École Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, Université de Lyon, Lyon, France.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Sletvold, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Divergent selection on flowering phenology but not on floral morphology between two closely related orchids2020In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 10, no 12, p. 5737-5747Article in journal (Refereed)
    Abstract [en]

    Closely related species often differ in traits that influence reproductive success, suggesting that divergent selection on such traits contribute to the maintenance of species boundaries. Gymnadenia conopsea ss. and Gymnadenia densiflora are two closely related, perennial orchid species that differ in (a) floral traits important for pollination, including flowering phenology, floral display, and spur length, and (b) dominant pollinators. If plant–pollinator interactions contribute to the maintenance of trait differences between these two taxa, we expect current divergent selection on flowering phenology and floral morphology between the two species. We quantified phenotypic selection via female fitness in one year on flowering start, three floral display traits (plant height, number of flowers, and corolla size) and spur length, in six populations of G. conopsea s.s. and in four populations of G. densiflora. There was indication of divergent selection on flowering start in the expected direction, with selection for earlier flowering in two populations of the early‐flowering G. conopsea s.s. and for later flowering in one population of the late‐flowering G. densiflora. No divergent selection on floral morphology was detected, and there was no significant stabilizing selection on any trait in the two species. The results suggest ongoing adaptive differentiation of flowering phenology, strengthening this premating reproductive barrier between the two species. Synthesis: This study is among the first to test whether divergent selection on floral traits contribute to the maintenance of species differences between closely related plants. Phenological isolation confers a substantial potential for reproductive isolation, and divergent selection on flowering time can thus greatly influence reproductive isolation and adaptive differentiation.

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  • 8.
    Chapurlat, Elodie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Anderson, Joseph
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Friberg, Magne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Lund Univ, Dept Biol, SE-22362 Lund, Sweden.
    Sletvold, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Conflicting selection on floral scent emission in the orchid Gymnadenia conopsea2019In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 222, no 4, p. 2009-2022Article in journal (Refereed)
    Abstract [en]

    Floral scent is a crucial trait for pollinator attraction. Yet only a handful of studies have estimated selection on scent in natural populations and no study has quantified the relative importance of pollinators and other agents of selection. In the fragrant orchid Gymnadenia conopsea, we used electroantennographic data to identify floral scent compounds detected by local pollinators and quantified pollinator-mediated selection on emission rates of 10 target compounds as well as on flowering start, visual display and spur length. Nocturnal pollinators contributed more to reproductive success than diurnal pollinators, but there was significant pollinator-mediated selection on both diurnal and nocturnal scent emission. Pollinators selected for increased emission of two compounds and reduced emission of two other compounds, none of which were major constituents of the total bouquet. In three cases, pollinator-mediated selection was opposed by nonpollinator-mediated selection, leading to weaker or no detectable net selection. Our study demonstrates that minor scent compounds can be targets of selection, that pollinators do not necessarily favour stronger scent signalling, and that some scent compounds are subject to conflicting selection from pollinators and other agents of selection. Hence, including floral scent traits into selection analysis is important for understanding the mechanisms behind floral evolution.

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  • 9.
    Chapurlat, Elodie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Sletvold, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Spatial variation in pollinator-mediated selection on phenology, floral display and spur length in the orchid Gymnadenia conopsea2015In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 208, no 4, p. 1264-1275Article in journal (Refereed)
    Abstract [en]

    Spatial variation in plant-pollinator interactions may cause variation in pollinator-mediated selection on floral traits, but to establish this link conclusively experimental studies are needed. We quantified pollinator-mediated selection on flowering phenology and morphology in four populations of the fragrant orchid Gymnadenia conopsea, and compared selection mediated by diurnal and nocturnal pollinators in two of the populations. Variation in pollinator-mediated selection explained most of the among-population variation in the strength of directional and correlational selection. Pollinators mediated correlational selection on pairs of display traits, and on one display trait and spur length, a trait affecting pollination efficiency. Only nocturnal pollinators selected for longer spurs, and mediated stronger selection on the number of flowers compared with diurnal pollinators in one population. The two types of pollinators caused correlational selection on different pairs of traits and selected for different combinations of spur length and number of flowers. The results demonstrate that spatial variation in interactions with pollinators may result in differences in directional and correlational selection on floral traits in a plant with a semi-generalized pollination system, and suggest that differences in the relative importance of diurnal and nocturnal pollinators can cause variation in selection.

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  • 10.
    Colautti, Robert I.
    et al.
    Queens Univ, Dept Biol, 116 Barrie St, Kingston, ON K7L 3N6, Canada..
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Anderson, Jill T.
    Univ Georgia, Dept Genet, 120 Green St, Athens, GA 30602 USA.;Univ Georgia, Odum Sch Ecol, 120 Green St, Athens, GA 30602 USA..
    Phenological shifts of native and invasive species under climate change: insights from the Boechera - Lythrum model2017In: 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)
    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'.

  • 11. Dalin, Peter
    et al.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Björkman, Christer
    Huttunen, Piritta
    Kärkkäinen, Katri
    Leaf trichome formation and plant resistance to herbivory2008In: Induced plant resistance to herbivory, Springer , 2008, p. 89-105Chapter in book (Other academic)
  • 12. Dittmar, Emily L.
    et al.
    Oakley, Christopher G.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Schemske, Douglas W.
    Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value2014In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 17, p. 4291-4303Article in journal (Refereed)
    Abstract [en]

    The genetic basis of phenotypic traits is of great interest to evolutionary biologists, but their contribution to adaptation in nature is often unknown. To determine the genetic architecture of flowering time in ecologically relevant conditions, we used a recombinant inbred line population created from two locally adapted populations of Arabidopsis thaliana from Sweden and Italy. Using these RILs, we identified flowering time QTL in growth chambers that mimicked the natural temperature and photoperiod variation across the growing season in each native environment. We also compared the genomic locations of flowering time QTL to those of fitness (total fruit number) QTL from a previous three-year field study. Ten total flowering time QTL were found, and in all cases, the Italy genotype caused early flowering regardless of the conditions. Two QTL were consistent across chamber environments, and these had the largest effects on flowering time. Five of the fitness QTL colocalized with flowering time QTL found in the Italy conditions, and in each case, the local genotype was favoured. In contrast, just two flowering time QTL found in the Sweden conditions colocalized with fitness QTL and in only one case was the local genotype favoured. This implies that flowering time may be more important for adaptation in Italy than Sweden. Two candidate genes (FLC and VIN3) underlying the major flowering time QTL found in the current study are implicated in local adaptation.

  • 13.
    Durán, Paloma
    et al.
    Max Planck Institute for Plant Breeding Research 50829 Cologne Germany;Cluster of Excellence on Plant Sciences (CEPLAS) Max Planck Institute for Plant Breeding Research 50829 Cologne Germany;LIPME Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique Castanet‐Tolosan 31326 France.
    Ellis, Thomas James
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Gregor Mendel Institute of Molecular Plant Sciences Austrian Academy of Sciences Doktor‐Bohr‐Gasse 3 1030 Vienna Austria.
    Thiergart, Thorsten
    Max Planck Institute for Plant Breeding Research 50829 Cologne Germany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Hacquard, Stéphane
    Max Planck Institute for Plant Breeding Research 50829 Cologne Germany;Cluster of Excellence on Plant Sciences (CEPLAS) Max Planck Institute for Plant Breeding Research 50829 Cologne Germany.
    Climate drives rhizosphere microbiome variation and divergent selection between geographically distant Arabidopsis populations2022In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 236, no 2, p. 608-621Article in journal (Refereed)
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  • 14. Ehlers, B. K.
    et al.
    Olesen, J. M.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Floral morphology and reproductive success in the orchid Epipactis helleborine: regional and local across-habitat variation2002In: Plant Systematics and Evolution, ISSN 0378-2697, E-ISSN 1615-6110, Vol. 236, no 1-2, p. 19-32Article in journal (Refereed)
    Abstract [en]

    The terrestrial orchid Epipactis helleborine is a morphologically variable species with a wide distribution in Europe. It is pollinated by social wasps, and most populations show the morphological characteristics of outcrossing species. However, local predominantly selfing subspecies and varieties have been documented from drier habitats. To document geographic variation in floral morphology, ability to produce seeds through autogamy, and reproductive success in E. helleborine, we sampled 13 populations from three geographic regions along a latitudinal gradient of c. 1000 km from northern to southern Sweden. In the southernmost region, populations in dry and mesic habitats were compared. Supplemental hand-pollination was conducted to determine whether among-population variation in fruit set could be explained by differences in the natural level of pollination, and whether any relationship between floral morphology and fruit production could be explained by interactions with pollinators. Bagging experiments showed no evidence of autogamy in any of the study populations. Number of flowers, pollinia removal and fruit set varied significantly among populations but did not differ among regions. Pollinia removal was positively correlated with population size and both pollinia removal and fruit set were lower in dry than in mesic habitats. At the level of the individual plant, the number of pollinia removed increased more rapidly with flower number than did number of fruits produced. The hand-pollination experiment indicated that the positive relationship between number of flowers and fruit production was due to a higher degree of pollen limitation in plants with few flowers than in plants with many flowers. The experiment also showed that variation in the level of pollen limitation could only partly explain variation in fruit set among populations.

  • 15.
    Ehrlén, Johan
    et al.
    Dept of Botany, Stockholm Univ..
    Käck, Sofia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Pollen limitation, seed predation and scape length in Primula farinosa2002In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 97, no 1, p. 45-51Article in journal (Refereed)
    Abstract [en]

    Floral display and reward production may affect the attractiveness of a plant to a range of interacting animals including pollinators, herbivores, and vectors of pathogenic fungi. The optimal floral phenotype should therefore depend on the relative importance of selection exerted by both mutualistic and antagonistic animals. The perennial, rosette herb Primula farinosa is polymorphic for scape length. Natural populations may include both plants with flowers displayed well above the ground (the long-scaped morph) and those with flowers positioned very close to the ground (the short-scaped morph). In this study, we conducted a field experiment to examine how the relative fitness of the two scape morphs is affected by interactions with pollinators and fruit predators in two different microhabitats (high and low vegetation). As predicted based on the difference in floral display, supplemental hand-pollination showed that fruit initiation was more strongly pollen-limited in the short-scaped than in the long-scaped morph, and that this difference was significantly larger in high than in low vegetation. Moreover, plants with a short scape experienced lower levels of fruit predation than plants with a long scape. Among open-pollinated controls, there was no significant difference in seed output between the two scape morphs. However, among plants receiving supplemental hand-pollination, short-scaped plants produced significantly more seeds than long-scaped plants. The results suggest that the positive and negative effects of a prominent floral display (increased pollination and seed predation, respectively) balance in the study population, but also that the short-scaped morph would have an advantage at higher pollination intensities. Spatial and temporal variation in pollinator activity and seed predation should result in associated variation in the relative fecundity of the two scape morphs.

  • 16.
    Ellis, Thomas James
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Gregor Mendel Inst Mol Plant Sci, Vienna, Austria.
    Postma, Froukje M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Oakley, Christopher G.
    Purdue Univ, Dept Bot & Plant Pathol, W Lafayette, IN 47907 USA.;Purdue Univ, Ctr Plant Biol, W Lafayette, IN 47907 USA.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Life-history trade-offs and the genetic basis of fitness in Arabidopsis thaliana2021In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 30, no 12, p. 2846-2858Article in journal (Refereed)
    Abstract [en]

    Resources allocated to survival cannot be used to increase fecundity, but the extent to which this trade-off constrains adaptation depends on overall resource status. Adaptation to local environmental conditions may therefore entail the evolution of traits that increase the amount of resources available to individuals (their resource status or ‘condition’). We examined the relative contribution of trade-offs and increased condition to adaptive evolution in a recombinant inbred line population of Arabidopsis thaliana planted at the native sites of the parental ecotypes in Italy and Sweden in 2 years. We estimated genetic correlations among fitness components based on genotypic means and explored their causes with QTL mapping. The local ecotype produced more seeds per fruit than did the non-local ecotype, reflected in stronger adaptive differentiation than was previously shown based on survival and fruit number only. Genetic correlations between survival and overall fecundity, and between number of fruits and number of seeds per fruit, were positive, and there was little evidence of a trade-off between seed size and number. Quantitative trait loci for these traits tended to map to the same regions of the genome and showed positive pleiotropic effects. The results indicate that adaptive differentiation between the two focal populations largely reflects the evolution of increased ability to acquire resources in the local environment, rather than shifts in the relative allocation to different life-history traits. Differentiation both in phenology and in tolerance to cold is likely to contribute to the advantage of the local genotype at the two sites.

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  • 17. Falahati-Anbaran, Mohsen
    et al.
    Lundemo, Sverre
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Stenoien, Hans K.
    Genetic consequences of seed banks in the perennial herb Arabidopsis lyrata subsp. petraea (Brassicaceae)2011In: American Journal of Botany, ISSN 0002-9122, E-ISSN 1537-2197, Vol. 98, no 9, p. 1475-1485Article in journal (Refereed)
    Abstract [en]

    Premise of the Study: Seed banks may increase the effective population size (N(e)) of plants as a result of elevated coalescence times for alleles residing in the populations. This has been empirically demonstrated in populations of the annual Arabidopsis thaliana, whereas comparable data for perennial species are currently lacking. We studied the contribution of seed banks to effective sizes of natural populations of the self-incompatible, perennial Arabidopsis lyrata subsp. petraea, a close relative of A. thaliana. Methods: Fourteen populations of A. lyrata collected throughout the Norwegian distribution range were analyzed using micro-satellite markers. Key Results: The genetic composition of seed-bank and aboveground cohorts was found to be highly similar, with little genetic differentiation between cohorts in most populations. However, the proportion of private alleles was higher in aboveground than in seed-bank cohorts. The presence of seed banks significantly increased total N(e), but the contribution from seed banks to overall N(e) were lower than the contribution from aboveground cohorts in most populations. Estimated historical N(e) values, reflecting the effective sizes of populations throughout the history of the species, were considerably higher than estimates of contemporary N(e), reflecting number of reproducing individuals within the past few generations. Conclusions: The results show that the seed bank contributes to total N(e) in the perennial herb A. lyrata. However, the contribution is similar to or lower than that of the above-ground fraction of the population and markedly weaker than that previously documented in the annual A. thaliana.

  • 18.
    Fogelqvist, Johan
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics.
    Niittyvuopio, Anne
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Savolainen, Outi
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics.
    Cryptic population genetic structure: the number of inferred clusters depends on sample size2010In: Molecular Ecology Resources, ISSN 1755-098X, Vol. 10, no 2, p. 314-323Article in journal (Refereed)
    Abstract [en]

    Clustering methods have been used extensively to unravel cryptic population genetic structure. We investigated the effect of the number of individuals sampled in each location on the resulting number of clusters. Our study was motivated by recent results in Arabidopsis thaliana: studies in which more than one individual was sampled per location apparently have led to a much higher number of clusters than studies where only one individual was sampled in each location, as is generally done in this species. We show, using computer simulations and microsatellite data in A. thaliana, that the number of sampled individuals indeed has a strong impact on the number of resulting clusters. This effect is smaller if the sampled populations have a hierarchical structure. In most cases, sampling 5-10 individuals per population should be enough. The results argue for abandoning the concept of 'accessions' in partially selfing organisms.

  • 19. Frenkel, Martin
    et al.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Jansson, Stefan
    Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming2009In: BMC Plant Biology, E-ISSN 1471-2229, Vol. 9, p. 12-Article in journal (Refereed)
    Abstract [en]

    Background. Plant performance is affected by the level of expression of PsbS, a key photoprotective protein involved in the process of feedback de-excitation (FDE), or the qE component of non-photochemical quenching, NPQ. Results. In studies presented here, under constant laboratory conditions the metabolite profiles of leaves of wild-type Arabidopsis thaliana and plants lacking or overexpressing PsbS were very similar, but under natural conditions their differences in levels of PsbS expression were associated with major changes in metabolite profiles. Some carbohydrates and amino acids differed ten-fold in abundance between PsbS-lacking mutants and over-expressers, with wild-type plants having intermediate amounts, showing that a metabolic shift had occurred. The transcriptomes of the genotypes also varied under field conditions, and the genes induced in plants lacking PsbS were similar to those reportedly induced in plants exposed to ozone stress or treated with methyl jasmonate (MeJA). Genes involved in the biosynthesis of JA were up-regulated, and enzymes involved in this pathway accumulated. JA levels in the undamaged leaves of field-grown plants did not differ between wild-type and PsbS-lacking mutants, but they were higher in the mutants when they were exposed to herbivory. Conclusion. These findings suggest that lack of FDE results in increased photooxidative stress in the chloroplasts of Arabidopsis plants grown in the field, which elicits a response at the transcriptome level, causing a redirection of metabolism from growth towards defence that resembles a MeJA/JA response.

  • 20.
    Gaudeul, Myriam
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Stenøien, Hans K.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Landscape structure, clonal propagation, and genetic diversity in Scandinavian populations of Arabidopsis lyrata (Brassicaceae)2007In: American Journal of Botany, ISSN 0002-9122, E-ISSN 1537-2197, Vol. 94, no 7, p. 1146-1155Article in journal (Refereed)
    Abstract [en]

    Colonization history, landscape structure, and environmental conditions may influence patterns of neutral genetic variation because of their effects on gene flow and reproductive mode. We compared variation at microsatellite loci within and among 26 Arabidopsis lyrata populations in two disjunct areas of its distribution in northern Europe (Norway and Sweden). The two areas probably share a common colonization history but differ in size (Norwegian range markedly larger than Swedish range), landscape structure (mountains vs. coast), and habitat conditions likely to affect patterns of gene flow and opportunities for sexual reproduction. Within-population genetic diversity was not related to latitude but was higher in Sweden than in Norway. Population differentiation was stronger among Norwegian than among Swedish populations (F-ST = 0.23 vs. F-ST = 0.18). The frequency of clonal propagation (proportion of identical multilocus genotypes) increased with decreasing population size, was higher in Norwegian than in Swedish populations, but was not related to altitude or substrate. Differences in genetic structure are discussed in relation to population characteristics and range size in the two areas. The results demonstrate that the possibility of clonal propagation should be considered when developing strategies for sampling and analyzing data in ecological and genetic studies of this emerging model species.

  • 21. Hambäck, PA
    et al.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Plant Ecology.
    Ericson, L
    Associational resistance: insect damage to purple loosestrife reduced in thickets of sweet gale2000In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 81, no 7, p. 1784-1794Article in journal (Refereed)
    Abstract [en]

    Associational resistance occurs when herbivore damage to a focal plant is reduced by the presence of other plant species. Neighboring plants can reduce herbivore damage (1) by their effects on the predator community, (2) by reducing the ability of herbivores to find their host plants, and (3) by reducing the time herbivores remain on their host plants. We examined how the presence of the aromatic low shrub Myrica gale and of predatory lady beetles affected herbivore damage and reproductive output in a population of the perennial herb Lythrum salicaria in northern Sweden. An observational study showed that L. salicaria growing in Myrica thickets were less damaged by herbivores, had a lower abundance of the monophagous, leaf-feeding, chrysomelid beetle Galerucella calmariensis, and had higher flower and seed production than L. salicaria outside Myrica thickets. To test whether these differences could be explained by (a) differences in some aspect of plant quality, or (b) differences in predator abundance, we placed potted L. salicaria within and outside Myrica thickets. To determine whether differences in the abundance of G. calmariensis were primarily the result of different rates of colonization or emigration, we marked adult beetles and placed them on a second set of potted plants in the two micro-habitats. The results show that differences in herbivore abundance, plant damage, and reproductive output between potted L. salicaria placed within and outside Myrica thickets were in the same direction and of the same magnitude as those observed for naturally occurring plants, indicating that the observed patterns were not an effect of differences in the chemical composition of the host plant. Moreover, we found no support for the hypothesis that a higher abundance of insect predators could explain the lower abundance of G. calmariensis on L. salicaria in Myrica thickets. On the contrary, lady beetles (Coccinella quinqempunctata and Coccinella septempunctata) were observed on a greater proportion of the plants placed outside the Myrica thickets. The monitoring of marked beetles indicated that differences in the abundance of G. calmariensis were the result of a markedly higher colonization rate and a somewhat lower emigration rate from L. salicaria outside Myrica thickets. Outside the Myrica thickets, the survival of G. calmariensis and the magnitude of herbivore damage were lower, and fruit and seed output were higher on plants with observations of lady beetles than on plants without lady beetles. The results indicate that the abundance of the specialist herbivore G. calmariensis, and the herbivore damage and reproductive output of its host plant, L. salicaria, are affected both by the presence of the nonhost Myrica and by predation from lady beetles. We suggest that the most likely mechanism causing decreased feeding on L. salicaria growing in Myrica thickets is that Myrica affects the ability of G. calmariensis to find its host, either through visual or olfactory interference.

  • 22. Handley, RJ
    et al.
    Ekbom, B
    Ågren, Jon
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Plant Ecology.
    Variation in trichome density and resistance against a specialist herbivore in natural populations of Arabidopsis thaliana2005In: Ecological Entomology, Vol. 30, p. 284-292Article in journal (Refereed)
  • 23.
    Harder, Lawrence D.
    et al.
    Univ Calgary, Dept Biol Sci, Calgary, AB T2N 1N4, Canada.
    Richards, Shane A.
    Univ Tasmania, Sch Nat Sci, Sandy Bay, Tas 7001, Australia.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Johnson, Steven D.
    Univ KwaZulu Natal Pietermaritzburg, Sch Life Sci, Ctr Funct Biodivers, Private Bag X01, ZA-3209 Scottsville, South Africa.
    Mechanisms of Male-Male Interference during Dispersal of Orchid Pollen2021In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 197, no 2, p. 250-265Article in journal (Refereed)
    Abstract [en]

    Siring success of flowering plants depends on the fates of male gametophytes, which compete for access to stigmas, stylar resources, and ovules. Although rarely considered, pollen may often compete during dispersal, affecting the processes required for export to stigmas: pollen pickup, transport, and deposition. We quantified dispersal interference by tracking bee-mediated dispersal of stained Anacamptis morio (Orchidaceae) pollen from individual donor flowers and inferred the affected dispersal mechanisms on the basis of the fit of a process-based model. During individual trials, all recipient flowers were either emasculated, precluding interference with donor pollen, or intact, adding potentially interfering pollen to the pollinator. The presence of competing pollinaria on bees reduced pickup of additional pollinaria, doubled the overall proportion of lost donor pollen, and reduced total pollen export by 27%. Interference specifically increased loss of donor pollen between successive flower visits and variation in deposition among trials, and it likely also reduced pollen contact with stigmas and pollen deposition when contact occurred. Thus, by altering pollen removal, transport, and deposition, male-male interference during pollen dispersal can significantly—and perhaps commonly—limit plant-siring success.

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  • 24. Huttunen, Piritta
    et al.
    Karkkainen, Katri
    Loe, Geir
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Rautio, Pasi
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Leaf trichome production and responses to defoliation and drought in Arabidopsis lyrata (Brassicaceae)2010In: Annales Botanici Fennici, ISSN 0003-3847, E-ISSN 1797-2442, Vol. 47, no 3, p. 199-207Article in journal (Refereed)
    Abstract [en]

    Leaf trichomes can protect plants against herbivory and drought, but can be costly to produce. Theory suggests that selection for reduced costs of resistance may result in the evolution of inducible defences. We quantified variation in tolerance to drought and defoliation, and tested the hypotheses that (a) tolerance is associated with cost, (b) leaf trichome production increases tolerance to drought, and (c) trichome production is increased in response to defoliation and drought stress in Arabidopsis lyrata (Brassicaceae). Eight maternal half-sib families were exposed to two watering regimes and four defoliation treatments in a factorial design. Tolerance to drought varied among families and was inversely related to leaf size, but was not related to trichome density. Family mean performance in the low-watering treatment tended to correlate negatively with that in the control treatment. Trichome production was not induced by defoliation or drought stress. The results suggest that there is genetic variation in tolerance to drought in the study population, that tolerance to drought is associated with a cost, and that trichome production does not increase tolerance to drought in A. lyrata.

  • 25.
    Jakobsson, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Padrón, Benigno
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Distance-dependent effects of invasive Lupinus polyphyllus on pollination and reproductive success of two native herbs2015In: Basic and Applied Ecology, ISSN 1439-1791, E-ISSN 1618-0089, Vol. 16, no 2, p. 120-127Article in journal (Refereed)
    Abstract [en]

    A comprehensive understanding of the effects of invasive plants on native species requires identification of both the mechanisms of interaction and the spatial scale over which they act. Indirect interactions involving mobile organisms such as pollinators are likely to be scale-dependent, yet most studies examining effects of invasive species on pollination of native plants have considered effects across a single distance between interacting species. We examined the effects of the invasive herb Lupinus polyphyllus on pollination of two native herbs using multiple distances between the invasive and the natives. We recorded pollinator visitation and seed production in the native herbs Lotus corniculatus and Lychnis viscaria at 0, 5 m or 200 m away from L. polyphyllus. To reduce the influence of confounding factors, we used experimentally established populations of the invasive and potted individuals of the natives. In the immediate vicinity to L. polyphyllus, visitation to L. corniculatus was higher than 200 m away, and seed production per flower was higher than 5 m and 200 m away. In L. viscaria, bumblebee visitation was higher adjacent to L. polyphyllus than 5 m and 200 m away, but total pollinator visitation and reproductive success did not vary with distance. The results indicate that L. polyphyllus facilitates pollination of the native plants, and that this occurs at a very local spatial scale as effects dropped off already at a distance of 5 m. Presence of L. polyphyllus could benefit both pollinators and pollination of native herbs, and these positive effects should be considered along with likely negative effects due to resource competition. Moreover, the results illustrate the necessity to consider scale-dependent effects when assessing the impact of invasive flowering plants on native pollination interactions.

  • 26.
    Jakobsson, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Distance to semi-natural grassland influences seed production of insect-pollinated herbs2014In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 175, no 1, p. 199-208Article in journal (Refereed)
    Abstract [en]

    Marginal grassland fragments, such as road verges and field margins, may act as important supplemental habitats for grassland plants in the modern agricultural landscape. However, abundance of pollinators in such fragments has been found to decline with distance to larger natural and semi-natural habitats, and this could have corresponding effects on plant pollination. In this study, we performed a field experiment on road verges with three insect-pollinated grassland herbs to examine the relationship between distance to semi-natural grassland and plant reproductive success in two landscapes with contrasting farming intensities. In Lychnis viscaria and Lotus corniculatus, seed production tended to decrease with increasing distance to semi-natural grassland, but only in the landscape with high farming intensity. Seed production in Armeria maritima spp. maritima decreased with distance in both landscapes. Although many studies have investigated effects of natural habitat on crop pollination, little is known about the impact on pollination in native plants. The results from this study indicate that management of semi-natural grasslands improves not only biodiversity within the actual grassland but also pollination of native plants in the surrounding agricultural landscape.

  • 27. Johnson, S.D.
    et al.
    Collin, C.L.
    Wissman, H.J.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Halvarsson, E
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Ågren, Jon
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Factors contributing to variation in seed production among remnant populations of the endangered daisy Gerbera aurantiaca2004In: Biotropica, Vol. 36, p. 148-155Article in journal (Refereed)
  • 28. Johnson, S.D.
    et al.
    Peter, C.I.
    Ågren, Jon
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    The effect of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio2004In: Proceedings of the Royal Society of London B, Vol. 271, p. 803-809Article in journal (Refereed)
  • 29. Johnson, Steven D.
    et al.
    Peter, Craig I.
    Nilsson, L. Anders
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Pollination success in a deceptive orchid is enhanced by co-ocurring rewarding magnet plants2003In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 84, no 11, p. 2919-2927Article in journal (Refereed)
    Abstract [en]

    It has been debated whether pollination success in nonrewarding plants that flower in association with nectar-producing plants will be diminished by competition for pollinator visits or, alternatively, enhanced through increased local abundance of pollinators (the magnet species effect). We experimentally evaluated these effects using the nonrewarding bumblebee-pollinated orchid Anacamptis morio and associated nectar-producing plants at a site in Sweden. Pollination success (estimated as pollen receipt and pollen removal) in A. morio was significantly greater for individuals translocated to patches of nectar-producing plants (Geum rivale and Allium schoenoprasum) than for individuals placed outside (20 m away) such patches. These results provide support for the existence of a facilitative magnet species effect in the interaction between certain nectar plants and A. morio. To determine the spatial scale of these interactions, we correlated the visitation rate to flowers of A. morio with the density of sympatric nectar plants in 1-m2 and 100-m2 plots centered around groups of translocated plants, and at the level of whole meadows (0.5–2 ha). Visitation rate to flowers of A. morio was not correlated with the 1-m2 patch density of G. rivale and A. schoenoprasum, but showed a significant positive relationship with density of these nectar plants in 100-m2 plots. In addition, visitation to flowers of A. morio was strongly and positively related to the density of A. schoenoprasum at the level of the meadow. Choice experiments showed that bees foraging on the purple flowers of A. schoenoprasum (a particularly effective magnet species) visit the purple flowers of A. morio more readily (47.6% of choices) than bees foraging on the yellow flowers of Lotus corniculatus (17% of choices). Overall similarity in flower color and shape may increase the probability that a pollinator will temporarily shift from a nectar-producing “magnet” plant to a nonrewarding plant. We discuss the possibility of a mimicry continuum between those orchids that exploit instinctive food-seeking behavior of pollinators and those that show an adaptive resemblance to nectar-producing plants.

  • 30. Johnson, Steven D.
    et al.
    Torninger, Erica
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Relationships between population size and pollen fates in a moth-pollinated orchid2009In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 5, no 2, p. 282-285Article in journal (Refereed)
    Abstract [en]

    Management of small plant populations requires an understanding of their reproductive ecology, particularly in terms of sensitivity to Allee effects. To address this issue, we explored how components of pollen transfer and pollination success of individual plants varied among 36 populations of the self-compatible moth-pollinated orchid Satyrium longicauda in South Africa. Mean fruit set, seed production, proportion of flowers with pollen deposited or removed and proportion of removed pollen that reached stigmas (approx. 8% in this species) were not significantly related to population size (range: 1–450 flowering individuals), density or isolation. Plants in small populations did, however, have significantly higher levels of pollinator-mediated self-pollination (determined using colour-labelled pollen) than those in larger populations. Our results suggest that small populations of this orchid species are resilient to Allee effects in terms of overall pollination success, although the higher levels of pollinator-mediated self-pollination in small populations may lead to inbreeding depression and long-term erosion of genetic diversity.

  • 31. Kivimäki, Maarit
    et al.
    Kärkkäinen, Katri
    Gauldeul, Myriam
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Løe, Geir
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Gene, phenotype and function: GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata2007In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 16, no 2, p. 453-462Article in journal (Refereed)
    Abstract [en]

    The molecular genetic basis of adaptive variation is of fundamental importance for evolutionary dynamics, but is still poorly known. Only in very few cases has the relationship between genetic variation at the molecular level, phenotype and function been established in natural populations. We examined the functional significance and genetic basis of a polymorphism in production of leaf hairs, trichomes, in the perennial herb Arabidopsis lyrata. Earlier studies suggested that trichome production is subject to divergent selection. Here we show that the production of trichomes is correlated with reduced damage from insect herbivores in natural populations, and using statistical methods developed for medical genetics we document an association between loss of trichome production and mutations in the regulatory gene GLABROUS1. Sequence data suggest that independent mutations in this regulatory gene have provided the basis for parallel evolution of reduced resistance to insect herbivores in different populations of A. lyrata and in the closely related Arabidopsis thaliana. The results show that candidate genes identified in model organisms provide a valuable starting point for analysis of the genetic basis of phenotypic variation in natural populations.

  • 32. Kärkkäinen, K
    et al.
    Løe, Geir
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Ågren, Jon
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Population structure in Arabidopsis lyrata: evidence for divergent selection on trichome production2004In: Evolution, Vol. 58, p. 2831-2836Article in journal (Refereed)
  • 33.
    Kärkkäinen, K.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology.
    Ågren, J.
    Genetic basis of trichome production in Arabidopsis lyrata.2002In: Hereditas, Vol. 136, p. 219-226Article in journal (Refereed)
  • 34.
    Külheim, Carsetn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Jansson, Stefan
    Rapid Regulation of Light Harvesting and Plant Fitness in the Field.2002In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 297, no 5578, p. 91-93Article in journal (Refereed)
    Abstract [en]

    We used Arabidopsis thaliana mutants to examine how a photosynthetic regulatory process, the qE-type or ΔpH-dependent nonphotochemical quenching, hereafter named feedback de-excitation, influences plant fitness in different light environments. We show that the feedback de-excitation is important for plant fitness in the field and in fluctuating light in a controlled environment but that it does not affect plant performance under constant light conditions. Our findings demonstrate that the feedback de-excitation confers a strong fitness advantage under field conditions and suggest that this advantage is due to the increase in plant tolerance to variation in light intensity rather than tolerance to high-intensity light itself.                      

  • 35.
    Laenen, Benjamin
    et al.
    Stockholm Univ, Sci Life Lab, Dept Ecol Environm & Plant Sci, SE-10691 Stockholm, Sweden..
    Tedder, Andrew
    Stockholm Univ, Sci Life Lab, Dept Ecol Environm & Plant Sci, SE-10691 Stockholm, Sweden..
    Nowak, Michael D.
    Stockholm Univ, Sci Life Lab, Dept Ecol Environm & Plant Sci, SE-10691 Stockholm, Sweden..
    Toräng, Per
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Wunder, Jörg
    Max Planck Inst Plant Breeding Res, D-50829 Cologne, Germany..
    Wötzel, Stefan
    Max Planck Inst Plant Breeding Res, D-50829 Cologne, Germany..
    Steige, Kim A.
    Stockholm Univ, Sci Life Lab, Dept Ecol Environm & Plant Sci, SE-10691 Stockholm, Sweden.;Univ Cologne, Inst Bot, Biozentrum, D-50674 Cologne, Germany..
    Kourmpetis, Yiannis
    Wageningen Univ & Res Ctr, Biometris, NL-6700 AC Wageningen, Netherlands.;Nestle Inst Hlth Sci, CH-1015 Lausanne, Switzerland..
    Odong, Thomas
    Wageningen Univ & Res Ctr, Biometris, NL-6700 AC Wageningen, Netherlands..
    Drouzas, Andreas D.
    Aristotle Univ Thessaloniki, Sch Biol, Thessaloniki 54124, Greece..
    Bink, Marco C. A. M.
    Wageningen Univ & Res Ctr, Biometris, NL-6700 AC Wageningen, Netherlands.;Hendrix Genet Res Technol & Serv, NL-5830 AC Boxmeer, Netherlands..
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Coupland, George
    Max Planck Inst Plant Breeding Res, D-50829 Cologne, Germany..
    Slotte, Tanja
    Stockholm Univ, Sci Life Lab, Dept Ecol Environm & Plant Sci, SE-10691 Stockholm, Sweden..
    Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina2018In: 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)
    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.

  • 36. Lee, Gwonjin
    et al.
    Sanderson, Brian J.
    Ellis, Thomas J.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Dilkes, Brian P.
    McKay, John K.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Oakley, Christopher G.
    A large-effect fitness trade-off across environments is explained by a single mutation affecting cold acclimation2024In: 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)
    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.

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  • 37.
    Lehndal, Lina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Hambäck, Peter
    Stockholm Univ, Dept Ecol Environm & Plant Sci, S-10691 Stockholm, Sweden.
    Ericson, Lars
    Umea Univ, Dept Ecol & Environm Sci, S-90187 Umea, Sweden.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Herbivory strongly influences among-population variation in reproductive output of Lythrum salicaria in its native range2016In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 180, no 4, p. 1159-1171Article in journal (Refereed)
    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.

  • 38.
    Lehndal, Lina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Herbivory Differentially Affects Plant Fitness in Three Populations of the Perennial Herb Lythrum salicaria along a Latitudinal Gradient2015In: PLOS ONE, E-ISSN 1932-6203, Vol. 10, no 9, article id e0135939Article in journal (Refereed)
    Abstract [en]

    Herbivory can negatively and selectively affect plant fitness by reducing growth, survival and reproductive output, thereby influencing plant population dynamics and evolution. We documented intensity of herbivory and experimentally examined its effect on survival, growth and reproductive output in three natural populations of the perennial herb Lythrum salicaria along a latitudinal gradient from southern to northernmost Sweden over two years. The intensity of herbivory and the effects of herbivory on plant fitness were strongest in the southern population and intermediate in the central population. The mean proportion of the leaf area removed ranged from 11% in the southern to 3% in the northern population. Herbivore removal increased plant height 1.5-fold in the southern and 1.2-fold in the central population, the proportion plants flowering 4-fold in the southern and 2-fold in the central population, and seed production per flower 1.6-fold in the southern and 1.2-fold in the central population, but did not affect plant fitness in the northern population. Herbivore removal thus affected the relative fecundity of plants in the three populations: In the control, seed output per plant was 8.6 times higher in the northern population compared to the southern population, whereas after herbivore removal it was 2.5 times higher in the southern population compared to the northern. Proportion of leaf area removed increased with plant size, but tolerance to damage did not vary with size. The results demonstrate that native herbivores may strongly affect the demographic structure of L. salicaria populations, and thereby shape geographic patterns of seed production. They further suggest that the strength of herbivore-mediated selection varies among populations and decreases towards the north.

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  • 39.
    Lehndal, Lina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Latitudinal variation in resistance and tolerance to herbivory in the perennial herb Lythrum salicaria is related to intensity of herbivory and plant phenology2015In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 28, no 3, p. 576-589Article in journal (Refereed)
    Abstract [en]

    Both the length of the growing season and the intensity of herbivory often vary along climatic gradients, which may result in divergent selection on plant phenology, and on resistance and tolerance to herbivory. In Sweden, the length of the growing season and the number of insect herbivore species feeding on the perennial herb Lythrum salicaria decrease from south to north. Previous common-garden experiments have shown that northern L. salicaria populations develop aboveground shoots earlier in the summer, and finish growth before southern populations do. We tested the hypotheses that resistance and tolerance to damage vary with latitude in L. salicaria, and are positively related to the intensity of herbivory in natural populations. We quantified resistance and tolerance of populations sampled along a latitudinal gradient by scoring damage from natural herbivores and fitness in a common-garden experiment in the field, and by documenting oviposition and feeding preference by specialist leaf beetles in a greenhouse experiment. Plant resistance decreased with latitude of origin, whereas plant tolerance increased. Oviposition and feeding preference in the greenhouse, and leaf damage in the common-garden experiment were negatively related to damage in the source populations. The latitudinal variation in resistance was thus consistent with reduced selection from herbivores towards the northern range margin of L. salicaria. Variation in tolerance may be related to differences in the timing of damage in relation to the seasonal pattern of plant growth, as northern genotypes have developed further than southern have when herbivores emerge in early summer.

  • 40. Leinonen, Päivi H.
    et al.
    Sandring, Saskia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Quilot, Bénédicte
    Clauss, Maria J.
    Mitchell-Olds, Thomas
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Savolainen, Outi
    Local adaptation in European populations of Arabidopsis lyrata (Brassicaceae)2009In: American Journal of Botany, ISSN 0002-9122, E-ISSN 1537-2197, Vol. 96, no 6, p. 1129-1137Article in journal (Refereed)
    Abstract [en]

    We studied local adaptation to contrasting environments usingan organism that is emerging as a model for evolutionary plantbiology—the outcrossing, perennial herb Arabidopsis lyratasubsp. petraea (Brassicaceae). With reciprocal transplant experiments,we found variation in cumulative fitness, indicating adaptivedifferentiation among populations. Nonlocal populations didnot have significantly higher fitness than the local population.Experimental sites were located in Norway (alpine), Sweden (coastal),and Germany (continental). At all sites after one year, thelocal population had higher cumulative fitness, as quantifiedby survival combined with rosette area, than at least one ofthe nonlocal populations. At the Norwegian site, measurementswere done for two additional years, and fitness differencespersisted. The fitness components that contributed most to differencesin cumulative fitness varied among sites. Relatively small rosettearea combined with a large number of inflorescences producedby German plants may reflect differentiation in life history.The results of the current study demonstrate adaptive populationdifferentiation in A. lyrata along a climatic gradient in Europe.The studied populations harbor considerable variation in severalcharacters contributing to adaptive population differentiation.The wealth of genetic information available makes A. lyrataa highly attractive system also for examining the functionaland genetic basis of local adaptation in plants.

  • 41.
    Løe, Geir
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Toräng, Per
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Gauldeul, Myriam
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Trichome production and spatiotemporal variation in herbivory in the perennial herb Arabidopsis lyrata2007In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 116, no 1, p. 134-142Article in journal (Refereed)
    Abstract [en]

    Allocation theory suggests that the optimal level of resistance against herbivores should vary with the risk of herbivory if allocation to resistance is costly. The perennial herb Arabidopsis lyrata has a genetically based polymorphism for- trichome production and occurs in a glabrous and a trichome-producing form. Leaf trichomes (hairs) can protect plants against insect herbivores, and may increase tolerance to drought and UV-radiation. To examine the functional significance of trichome production, we documented the frequency of glabrous plants and damage by insect herbivores in 30 A. lyrata populations in Sweden and Norway. The proportion of glabrous plants ranged from 0.10 to 0.71 (median = 0.44) in polymorphic populations; 7 of 12 populations in Norway and 14 of 18 populations in Sweden were monomorphic glabrous, i.e. with fewer than 5% trichome-producing plants. The mean proportion of the leaf area removed by herbivores varied substantially among populations and years. With few exceptions, glabrous plants were more damaged than trichome-producing plants in polymorphic populations. The intensity of herbivory quantified as the mean damage to glabrous plants tended to be higher in polymorphic populations than in populations monomorphic for the glabrous morph and was higher in Sweden than in Norway. In Norway, both the magnitude of herbivore damage and the frequency of trichome-producing plants tended to decrease with increasing altitude. The results indicate that leaf trichomes contribute to resistance against herbivorous insects in A. lyrata, and suggest that herbivore-mediated selection contributes to the maintenance of the polymorphism in trichome production.

  • 42.
    Menzel, Mandy
    et al.
    Lund Univ, Lund, Sweden.
    Sletvold, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Hansson, Bengt
    Lund Univ, Lund, Sweden.
    Inbreeding Affects Gene Expression Differently in Two Self-Incompatible Arabidopsis lyrata Populations with Similar Levels of Inbreeding Depression2015In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 32, no 8, p. 2036-2047Article in journal (Refereed)
    Abstract [en]

    Knowledge of which genes and pathways are affected by inbreeding may help understanding the genetic basis of inbreeding depression, the potential for purging (selection against deleterious recessive alleles), and the transition from outcrossing to selfing. Arabidopsis lyrata is a predominantly self-incompatible perennial plant, closely related to the selfing model species A. thaliana. To examine how inbreeding affects gene expression, we compared the transcriptome of experimentally selfed and outcrossed A. lyrata originating from two Scandinavian populations that express similar inbreeding depression for fitness ((partial derivative approximate to 0.80). The number of genes significantly differentially expressed between selfed and outcrossed individuals were 2.5 times higher in the Norwegian population (approximate to 500 genes) than in the Swedish population (approximate to 200 genes). In both populations, a majority of genes were upregulated on selfing (approximate to 80%). Functional annotation analysis of the differentially expressed genes showed that selfed offspring were characterized by 1) upregulation of stress-related genes in both populations and 2) upregulation of photosynthesis-related genes in Sweden but downregulation in Norway. Moreover, we found that reproduction-and pollination-related genes were affected by inbreeding only in Norway. We conclude that inbreeding causes both general and population-specific effects. The observed common effects suggest that inbreeding generally upregulates rather than downregulates gene expression and affects genes associated with stress response and general metabolic activity. Population differences in the number of affected genes and in effects on the expression of photosynthesis-related genes show that the genetic basis of inbreeding depression can differ between populations with very similar levels of inbreeding depression.

  • 43. Monroe, J. Grey
    et al.
    Murray, Kevin D.
    Xian, Wenfei
    Srikant, Thanvi
    Carbonell-Bejerano, Pablo
    Becker, Claude
    Lensink, Mariele
    Exposito-Alonso, Moises
    Klein, Marie
    Hildebrandt, Julia
    Neumann, Manuela
    Kliebenstein, Daniel
    Weng, Mao-Lun
    Imbert, Eric
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Rutter, Matthew T.
    Fenster, Charles B.
    Weigel, Detlef
    Reply to: Re-evaluating evidence for adaptive mutation rate variation2023In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 619, no 7971, p. E57-E60Article in journal (Refereed)
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  • 44.
    Monroe, J. Grey
    et al.
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany.;Univ Calif Davis, Dept Plant Sci, Davis, CA 95616 USA..
    Srikant, Thanvi
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany..
    Carbonell-Bejerano, Pablo
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany..
    Becker, Claude
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany.;Ludwig Maximilians Univ Munchen, Fac Biol, Martinsried, Germany..
    Lensink, Mariele
    Univ Calif Davis, Dept Plant Sci, Davis, CA 95616 USA..
    Exposito-Alonso, Moises
    Carnegie Inst Sci, Dept Plant Biol, 290 Panama St, Stanford, CA 94305 USA.;Stanford Univ, Dept Biol, Stanford, CA 94305 USA..
    Klein, Marie
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany.;Univ Calif Davis, Dept Plant Sci, Davis, CA 95616 USA..
    Hildebrandt, Julia
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany..
    Neumann, Manuela
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany..
    Kliebenstein, Daniel
    Univ Calif Davis, Dept Plant Sci, Davis, CA 95616 USA..
    Weng, Mao-Lun
    Westfield State Univ, Dept Biol, Westfield, MA USA..
    Imbert, Eric
    Univ Montpellier, ISEM, Montpellier, France..
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Rutter, Matthew T.
    Coll Charleston, Dept Biol, Charleston, SC 29401 USA..
    Fenster, Charles B.
    South Dakota State Univ, Oak Lake Field Stn, Brookings, SD 57007 USA..
    Weigel, Detlef
    Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany..
    Mutation bias reflects natural selection in Arabidopsis thaliana2022In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 602, no 7895, p. 101-105Article in journal (Refereed)
    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.

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  • 45.
    Nilsson, Emil
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Ågren, Jon
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Plant Ecology. Växtekologi.
    Population size, female fecundity, and sex ratio variation in gynodioecious Plantago maritima2006In: Journal of Evolutionary Biology, Vol. 19, p. 825-833Article in journal (Refereed)
  • 46. Oakley, C. G.
    et al.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Schemske, D. W.
    Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana2015In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 115, no 1, p. 73-82Article in journal (Refereed)
    Abstract [en]

    Understanding the causes and architecture of genetic differentiation between natural populations is of central importance in evolutionary biology. Crosses between natural populations can result in heterosis if recessive or nearly recessive deleterious mutations have become fixed within populations because of genetic drift. Divergence between populations can also result in outbreeding depression because of genetic incompatibilities. The net fitness consequences of between-population crosses will be a balance between heterosis and outbreeding depression. We estimated the magnitude of heterosis and outbreeding depression in the highly selfing model plant Arabidopsis thaliana, by crossing replicate line pairs from two sets of natural populations (C <-> R, B <-> S) separated by similar geographic distances (Italy <-> Sweden). We examined the contribution of different modes of gene action to overall differences in estimates of lifetime fitness and fitness components using joint scaling tests with parental, reciprocal F-1 and F-2, and backcross lines. One of these population pairs (C <-> R) was previously demonstrated to be locally adapted, but locally maladaptive quantitative trait loci were also found, suggesting a role for genetic drift in shaping adaptive variation. We found markedly different genetic architectures for fitness and fitness components in the two sets of populations. In one (C <-> R), there were consistently positive effects of dominance, indicating the masking of recessive or nearly recessive deleterious mutations that had become fixed by genetic drift. The other set (B <-> S) exhibited outbreeding depression because of negative dominance effects. Additional studies are needed to explore the molecular genetic basis of heterosis and outbreeding depression, and how their magnitudes vary across environments.

  • 47.
    Oakley, Christopher G.
    et al.
    Michigan State Univ, Dept Plant Biol, E Lansing, MI 48824 USA;Purdue Univ, Dept Bot & Plant Pathol, Ctr Plant Biol, W Lafayette, IN 47907 USA.
    Lundemo, Sverre
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. WWF Norway, Oslo, Norway.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Schemske, Douglas W.
    Michigan State Univ, Dept Plant Biol, WK Kellogg Biol Stn, E Lansing, MI 48824 USA.
    Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana2019In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 32, no 6, p. 592-603Article in journal (Refereed)
    Abstract [en]

    The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter-population crosses may therefore exhibit heterosis (increased fitness relative to intra-population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs of Arabidopsis thaliana from 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (median F-ST = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.

  • 48. Oakley, Christopher G.
    et al.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Atchison, Rachel A.
    Schemske, Douglas W.
    QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs2014In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 17, p. 4304-4315Article in journal (Refereed)
    Abstract [en]

    Local adaptation, defined as higher fitness of local vs. nonlocal genotypes, is commonly identified in reciprocal transplant experiments. Reciprocally adapted populations display fitness trade-offs across environments, but little is known about the traits and genes underlying fitness trade-offs in reciprocally adapted populations. We investigated the genetic basis and adaptive significance of freezing tolerance using locally adapted populations of Arabidopsis thaliana from Italy and Sweden. Previous reciprocal transplant studies of these populations indicated that subfreezing temperature is a major selective agent in Sweden. We used quantitative trait locus (QTL) mapping to identify the contribution of freezing tolerance to previously demonstrated local adaptation and genetic trade-offs. First, we compared the genomic locations of freezing tolerance QTL to those for previously published QTL for survival in Sweden, and overall fitness in the field. Then, we estimated the contributions to survival and fitness across both field sites of genotypes at locally adaptive freezing tolerance QTL. In growth chamber studies, we found seven QTL for freezing tolerance, and the Swedish genotype increased freezing tolerance for five of these QTL. Three of these colocalized with locally adaptive survival QTL in Sweden and with trade-off QTL for overall fitness. Two freezing tolerance QTL contribute to genetic trade-offs across environments for both survival and overall fitness. A major regulator of freezing tolerance, CBF2, is implicated as a candidate gene for one of the trade-off freezing tolerance QTL. Our study provides some of the first evidence of a trait and gene that mediate a fitness trade-off in nature.

  • 49.
    Olsson, K.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Ecological Botany.
    Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria.2002In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 15, no 6, p. 983-996 Article in journal (Refereed)
    Abstract [en]

     In plants with a wide distribution, phenological characters can be expected to vary clinally along climatic gradients, whereas other characters important for adaptation to local biotic and abiotic factors may vary in a more mosaic fashion. We used common-garden experiments and controlled crosses to examine population differentiation in phenology, life history and morphology in the perennial herb Lythrum salicaria along a latitudinal transect through Sweden (57°N to 66°N). Northern populations initiated growth and flowering earlier, flowered for a shorter period, were shorter, produced more and larger winter buds, and were older at first reproduction than southern populations. Flower morphology varied significantly among populations, but was, with the exception of calyx length, not significantly related to latitude of origin. Survival in the common garden (at 63°49′N) was positively correlated with latitude of origin and the size and number of winter buds produced in the preceding year. The results suggest that the among-population differences in phenology and life history have evolved in response to latitudinal variation in length of the growing season. Further studies are required to determine whether population differentiation in flower morphology is maintained by selection.

  • 50.
    Opedal, Øystein H.
    et al.
    Department of Biology, Biodiversity Unit, Lund University, Lund 223 62, Sweden.
    Armbruster, W. Scott
    School of Biological Sciences, University of Portsmouth, Portsmouth PO1 2DY, UK;Institute of Arctic Biology, University of Alaska, Fairbanks, AK 99775.
    Hansen, Thomas F.
    Department of Biology, Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo 0316, Norway.
    Holstad, Agnes
    Department of Biology, Centre for Biodiversity Dynamics, Norwegian University of Science and Technology, Trondheim 7491, Norway.
    Pélabon, Christophe
    Department of Biology, Centre for Biodiversity Dynamics, Norwegian University of Science and Technology, Trondheim 7491, Norway.
    Andersson, Stefan
    Department of Biology, Biodiversity Unit, Lund University, Lund 223 62, Sweden.
    Campbell, Diane R.
    Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697.
    Caruso, Christina M.
    Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.
    Delph, Lynda F.
    Department of Biology, Indiana University, Bloomington, IN 47405.
    Eckert, Christopher G.
    Department of Biology, Queen’s University, Kingston, ON K7L 3N6, Canada.
    Lankinen, Åsa
    Department of Plant Protection Biology, Swedish University of Agricultural Sciences, 234 22 Lomma, Sweden.
    Walter, Greg M.
    School of Biological Sciences, Monash University, Melbourne 3800, Australia.
    Ågren, Jon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Bolstad, Geir H.
    Norwegian Institute for Nature Research, Trondheim 7485, Norway.
    Evolvability and trait function predict phenotypic divergence of plant populations2023In: 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)
    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.

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