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Selection during Early Life Stages and Local Adaptation in Arabidopsis thaliana
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Organisms are often adapted to their local environment, but the role of early life stages in adaptive differentiation among populations remains poorly known. The aim of my thesis was to investigate the contribution of early life stages to the magnitude and genetic basis of local adaptation, and to identify the underlying adaptive traits. For this, I used two natural populations of the annual plant Arabidopsis thaliana from Italy and Sweden, and a Recombinant Inbred Line (RIL) population derived from a cross between these populations. By combining greenhouse and field experiments, Quantitative Trait Loci (QTL) mapping, and path analysis, I examined (1) the genetic basis of seed dormancy, (2) the contribution of differential seedling establishment to local adaptation, (3) among-year variation in selection during seedling establishment, (4) direct and indirect effects of seed dormancy and timing of germination on fitness, and (5) the adaptive value of the seed bank.

I found that both the level and the genetic basis of seed dormancy were affected by the maternal environment. One major-effect QTL was identified in all maternal environments, which overlaps with the dormancy gene DELAY OF GERMINATION 1 (DOG1).

Selection through seedling establishment success contributed strongly to local adaptation and genetic tradeoffs, and varied among years. Variation in seedling establishment and overall fitness among RILs could be explained by genetically based differences in seed dormancy and timing of germination. Seed dormancy affected fitness throughout the life cycle, by affecting the proportion of germinated seeds, and indirectly via effects on timing of germination, plant size and flowering time.

My results suggest that a considerable portion of A. thaliana seeds enter the seed bank. I found genetic differences in dormancy cycling behaviour between the two populations, which could contribute to local adaptation. The value of a seed bank should be higher at the Swedish study site than at the Italian study site due to lower rate of seed mortality in the soil.

Overall, the results of this thesis demonstrate that early life stages contribute strongly to both the magnitude and the genetics of local adaptation.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. , 51 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1425
Keyword [en]
Dormancy cycling, Germination timing, Maternal effects, Natural variation, QTL mapping, Seed bank, Seed dormancy, Structural Equation Modeling
National Category
Evolutionary Biology Ecology Botany
Research subject
Biology with specialization in Ecological Botany
Identifiers
URN: urn:nbn:se:uu:diva-302862ISBN: 978-91-554-9687-6 (print)OAI: oai:DiVA.org:uu-302862DiVA: diva2:968060
Public defence
2016-10-28, Zootissalen, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2016-10-05 Created: 2016-09-12 Last updated: 2016-10-11
List of papers
1. Maternal environment affects the genetic basis of seed dormancy in Arabidopsis thaliana
Open this publication in new window or tab >>Maternal environment affects the genetic basis of seed dormancy in Arabidopsis thaliana
2015 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 24, no 4, 785-797 p.Article in journal (Refereed) Published
Abstract [en]

The genetic basis of seed dormancy, a key life history trait important for adaptive evolution in plant populations, has yet been studied only using seeds produced under controlled conditions in greenhouse environments. However, dormancy is strongly affected by maternal environmental conditions, and interactions between seed genotype and maternal environment have been reported. Consequently, the genetic basis of dormancy of seeds produced under natural field conditions remains unclear. We examined the effect of maternal environment on the genetic architecture of seed dormancy using a recombinant inbred line (RIL) population derived from a cross between two locally adapted populations of Arabidopsis thaliana from Italy and Sweden. We mapped quantitative trait loci (QTL) for dormancy of seeds produced in the greenhouse and at the native field sites of the parental genotypes. The Italian genotype produced seeds with stronger dormancy at fruit maturation than did the Swedish genotype in all three environments, and the maternal field environments induced higher dormancy levels compared to the greenhouse environment in both genotypes. Across the three maternal environments, a total of nine dormancy QTL were detected, three of which were only detected among seeds matured in the field, and six of which showed significant QTLxmaternal environment interactions. One QTL had a large effect on dormancy across all three environments and colocalized with the candidate gene DOG1. Our results demonstrate the importance of studying the genetic basis of putatively adaptive traits under relevant conditions.

Keyword
adaptation, Arabidopsis thaliana, genotype-by-environment interactions, maternal effects, quantitative trait loci mapping, seed dormancy
National Category
Ecology Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-248202 (URN)10.1111/mec.13061 (DOI)000349819300008 ()25640699 (PubMedID)
Available from: 2015-03-31 Created: 2015-03-30 Last updated: 2017-12-04Bibliographically approved
2. Early life stages contribute strongly to local adaptation in Arabidopsis thaliana
Open this publication in new window or tab >>Early life stages contribute strongly to local adaptation in Arabidopsis thaliana
2016 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 113, no 27, 7590-7595 p.Article in journal (Refereed) Published
Abstract [en]

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

Keyword
adaptive differentiation, divergent selection, genetic tradeoff, pleiotropy, QTL mapping
National Category
Botany Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-300043 (URN)10.1073/pnas.1606303113 (DOI)000379021700079 ()27330113 (PubMedID)
Available from: 2016-08-02 Created: 2016-08-02 Last updated: 2017-11-28Bibliographically approved
3. Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana
Open this publication in new window or tab >>Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-302861 (URN)
External cooperation:
Available from: 2016-09-12 Created: 2016-09-12 Last updated: 2016-09-12
4. Seed dormancy cycling and mortality differ between two locally adapted populations of Arabidopsis thaliana
Open this publication in new window or tab >>Seed dormancy cycling and mortality differ between two locally adapted populations of Arabidopsis thaliana
2016 (English)In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 117, no 2, 249-256 p.Article in journal (Refereed) Published
Abstract [en]

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

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

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