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Tracing selection and adaptation along an environmental gradient in Populus tremula
Umeå University, Faculty of Science and Technology, Ecology and Environmental Science. (Evolutionär Ekologi)
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The distribution of the expressed genotype is moved around in the population over time byevolution. Natural selection is one of the forces that act on the phenotype to change the patterns ofnucleotide variation underlying those distributions. How the phenotype changes over aheterogeneous environment describes the type of evolutionary force acting on this trait and thisshould be reflected in the variation at loci underlying this trait. While the variation in phenotypesand at the nucleotide level in a population indicates the same evolutionary force, it does notnecessarily mean that they are connected. In natural populations the continuous shifting of geneticmaterial through recombination events break down possible associations between loci facilitates theexamination of possible causal loci to single base pair differences in DNA-sequences. Connecting thegenotype and the phenotype thus provides an important step in the understanding the geneticarchitecture of complex traits and the forces that shape the observed patterns.This thesis examines the European aspen, Populus tremula, sampled from subpopulations overan extensive latitudinal gradient covering most of Sweden. Results show a clear geneticdifferentiation in the timing of bud set, a measure of the autumnal cessation of growth, betweendifferent parts of Sweden pointing at local adaptation. In the search for candidate genes thatunderlie the local adaptation found, most genes (25) in the photoperiodic gene network wereexamined for signals of selection. Genes in the photoperiodic network show an increase in theheterogeneity of differentiation between sampled subpopulations in Sweden. Almost half (12) of theexamined genes are under some form of selection. Eight of these genes show positive directionalselection on protein evolution and the gene that code for a photoreceptor, responsible for mediatingchanging light conditions to downstream targets in the network, has the hallmarks of a selectivesweep. The negative correlation between positive directional selection and synonymous diversityindicates that the majority of the photoperiod gene network has undergone recurrent selectivesweeps. A phenomenon that likely has occurred when P. tremula has readapted to the northern lightregimes during population expansion following retracting ice between periods of glaciations. Two ofthe genes under selection also have single nucleotide polymorphisms (SNP) that associate with budset, two in the PHYB2 gene and one in the LHY2 gene. Furthermore, there is an additional SNP inLHY1 that explain part of the variation in timing of bud set, despite the lack of a signal of selection atthe LHY1 gene. Together these SNPs explain 10-15% of the variation in the timing of bud set and 20-30% more if accounting for the positive co-variances between SNPs. There is thus rather extensiveevidence that genes in the photoperiod gene network control the timing of bud set, and reflect localadaptation in this trait.

Place, publisher, year, edition, pages
Umeå: Institutionen för Ekologi, miljö och geovetenskap, Umeå universitet , 2009. , p. 42
Keywords [en]
Local adaptation, Selection, genetic differentiation, QST, FST, Association study, frequency spectra, recurrent hitchhiking, selective sweep, Tree, Populus, natural selection, quantitative genetics
National Category
Ecology
Research subject
Population Biology; Genetics
Identifiers
URN: urn:nbn:se:umu:diva-30123ISBN: 978-91-7264-907-1 (print)OAI: oai:DiVA.org:umu-30123DiVA, id: diva2:279991
Public defence
2010-01-16, Stora Hörsalen KBC, KB3B1, Umeå Universitet, KBC, Linnaeus väg 6, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2009-12-17 Created: 2009-12-07 Last updated: 2018-06-08Bibliographically approved
List of papers
1. Natural phenological variation in aspen (Populus tremula): the SwAsp collection
Open this publication in new window or tab >>Natural phenological variation in aspen (Populus tremula): the SwAsp collection
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2008 (English)In: Tree Genetics & Genomes, ISSN 1614-2942, Vol. 4, p. 279-292Article in journal (Refereed) Published
Abstract [en]

The genus Populus is currently the main model system for genetic, genomic, and physiological research in trees. Phenotypic variation in aspen (Populus tremula) populations growing in different environments across Sweden is expected to reflect genetic variation that is important for local adaptation. To analyze such natural phenotypic and genetic variation, the Swedish Aspen (SwAsp) Collection was established. Trees were taken from 12 different populations across Sweden, from 56° to 66° latitude north and planted in two common gardens in Ekebo (55.9°N) and Sävar (63.4°N). Data related to phenological and growth traits were collected during the second year of growth. Some traits like the date of bud set and leaf area duration showed strong clinal variation patterns with latitude in both field trials, but the date of bud flush did not change along a latitudinal cline. The phenological traits showed moderate within-populations heritabilities, although growth traits showed weaker clinal patterns and lower heritabilities than the phenological traits. This research forms the starting point for the development of the SwAsp collection, a resource facilitating analysis of the natural genetic variation in aspen, the elucidation of the structure and dynamics of aspen populations, and the future identification of the genes controlling adaptive traits using association mapping of selected candidate genes.

Place, publisher, year, edition, pages
SpringerLink, 2008
Keywords
Populus tremula, Natural variation, Phenology
Identifiers
urn:nbn:se:umu:diva-11481 (URN)10.1007/s11295-007-0108-y (DOI)2-s2.0-38949171308 (Scopus ID)
Available from: 2009-01-09 Created: 2009-01-09 Last updated: 2023-03-24Bibliographically approved
2. Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits
Open this publication in new window or tab >>Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits
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2007 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 61, p. 2849-2860Article in journal (Refereed) Published
Abstract [en]

A correct timing of growth cessation and dormancy induction represents a critical ecological and evolutionary trade-off between survival and growth in most forest trees (Rehfeldt et al. 1999; Horvath et al. 2003; Howe et al. 2003). We have studied the deciduous tree European Aspen (Populus tremula) across a latitudinal gradient and compared genetic differentiation in phenology traits with molecular markers. Trees from 12 different areas covering 10 latitudinal degrees were cloned and planted in two common gardens. Several phenology traits showed strong genetic differentiation and clinal variation across the latitudinal gradient, with QST values generally exceeding 0.5. This is in stark contrast to genetic differentiation at several classes of genetic markers (18 neutral SSRs, 7 SSRs located close to phenology candidate genes and 50 SNPs from five phenology candidate genes) that all showed FST values around 0.015. We thus find strong evidence for adaptive divergence in phenology traits across the latitudinal gradient. However, the strong population structure seen at the quantitative traits is not reflected in underlying candidate genes. This result fit theoretical expectations that suggest that genetic differentiation at candidate loci is better described by FST at neutral loci rather than by QST at the quantitative traits themselves.

Place, publisher, year, edition, pages
Wiley InterScience, 2007
Keywords
clinal variation, gene flow, genetic markers, local adaptation, population structure
Identifiers
urn:nbn:se:umu:diva-17678 (URN)10.1111/j.1558-5646.2007.00230.x (DOI)17908247 (PubMedID)2-s2.0-36549060068 (Scopus ID)
Available from: 2007-12-07 Created: 2007-12-07 Last updated: 2023-03-24Bibliographically approved
3. Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula).
Open this publication in new window or tab >>Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula).
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2006 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 172, no 3, p. 1845-53Article in journal (Refereed) Published
Abstract [en]

The initiation of growth cessation and dormancy represents a critical ecological and evolutionary trade-off between survival and growth in most forest trees. The most important environmental cue regulating the initiation of dormancy is a shortening of the photoperiod and phytochrome genes have been implicated in short-day-induced bud set and growth cessation in Populus. We characterized patterns of DNA sequence variation at the putative candidate gene phyB2 in 4 populations of European aspen (Populus tremula) and scored single-nucleotide polymorphisms in an additional 12 populations collected along a latitudinal gradient in Sweden. We also measured bud set from a subset of these trees in a growth chamber experiment. Buds set showed significant clinal variation with latitude, explaining ~90% of the population variation in bud set. A sliding-window scan of phyB2 identified six putative regions with enhanced population differentiation and four SNPs showed significant clinal variation. The clinal variation at individual SNPs is suggestive of an adaptive response in phyB2 to local photoperiodic conditions. Three of four SNPs showing clinal variation were located in regions with excessive genetic differentiation, demonstrating that searching for regions of high genetic differentiation can be useful for identifying sites putatively involved in local adaptation.

Place, publisher, year, edition, pages
Pittsburgh, Pennsylvania, USA: the Genetics Society of America, 2006
Identifiers
urn:nbn:se:umu:diva-14211 (URN)10.1534/genetics.105.047522 (DOI)16361240 (PubMedID)2-s2.0-33645229343 (Scopus ID)
Available from: 2007-05-24 Created: 2007-05-24 Last updated: 2023-03-24Bibliographically approved
4. Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 Locus in European aspen (Populus tremula, Salicaceae).
Open this publication in new window or tab >>Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 Locus in European aspen (Populus tremula, Salicaceae).
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2008 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 178, no 4, p. 2217-26Article in journal (Refereed) Published
Abstract [en]

We investigated the utility of association mapping to dissect the genetic basis of naturally occurring variation in bud phenology in European aspen (Populus tremula). With this aim, we surveyed nucleotide polymorphism in 13 fragments spanning an 80-kb region surrounding the phytochrome B2 (phyB2) locus. Although polymorphism varies substantially across the phyB2 region, we detected no signs for deviations from neutral expectations. We also identified a total of 41 single nucleotide polymorphisms (SNPs) that were subsequently scored in a mapping population consisting of 120 trees. We identified two nonsynonymous SNPs in the phytochrome B2 gene that were independently associated with variation in the timing of bud set and that explained between 1.5 and 5% of the observed phenotypic variation in bud set. Earlier studies have shown that the frequencies of both these SNPs vary clinally with latitude. Linkage disequilibrium across the region was low, suggesting that the SNPs we identified are strong candidates for being causally linked to variation in bud set in our mapping populations. One of the SNPs (T608N) is located in the "hinge region," close to the chromophore binding site of the phyB2 protein. The other SNP (L1078P) is located in a region supposed to mediate downstream signaling from the phyB2 locus. The lack of population structure, combined with low levels of linkage disequilibrium, suggests that association mapping is a fruitful method for dissecting naturally occurring variation in Populus tremula.

Place, publisher, year, edition, pages
Pittsburgh, Pennsylvania, USA: the Genetics Society of America, 2008
Identifiers
urn:nbn:se:umu:diva-9659 (URN)10.1534/genetics.107.082354 (DOI)18245834 (PubMedID)2-s2.0-45849093336 (Scopus ID)
Available from: 2008-05-09 Created: 2008-05-09 Last updated: 2023-03-24Bibliographically approved
5. Adaptive evolution of the Populus tremula photoperiod pathway
Open this publication in new window or tab >>Adaptive evolution of the Populus tremula photoperiod pathway
2011 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 20, no 7, p. 1463-1474Article in journal (Refereed) Published
Abstract [en]

Environmental cues entrain the circadian clock, a core component of the photoperiod pathway in plants, to daily and seasonal changes. The circadian clock mediates input signals from light and temperature receptors to downstream target genes through feedback loops. Several studies have shown that a correct timing of the circadian system is a fitness advantage and genes in photoperiod network have been implied to evolve in response to the diversifying selection in heterogeneous environment. In an attempt to quantify the extent of the historical patterns of selection on genes in the photoperiod pathway in the widely distributed tree species European aspen (Populus tremula) we obtained sequences for twenty-five of the genes in the network and these genes were compared to patterns of nucleotide diversity in 77 randomly chosen genes from across the genome of P. tremula. We found a significant reduction in synonymous diversity in photoperiod genes while non-synonymous diversity was in line with data from control genes. A substantial fraction of the genes show signs of selection, with eight genes showing signs of rapid protein evolution. In contrast to our expectations, genes closely associated with the core circadian clock show rapid protein evolution despite their central position in the pathway. Furthermore, selection on non-synonymous mutations is negatively correlated with synonymous diversity across all genes, indicating the action of recurrent selective sweeps.

Keywords
recurrent hitch-hiking, selection, populus, natural selection, sweep
National Category
Other Biological Topics Genetics
Research subject
Genetics
Identifiers
urn:nbn:se:umu:diva-30355 (URN)10.1111/j.1365-294X.2011.05014.x (DOI)2-s2.0-79953043079 (Scopus ID)
Available from: 2009-12-17 Created: 2009-12-17 Last updated: 2023-03-24Bibliographically approved
6. Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula Photoperiodic Pathway
Open this publication in new window or tab >>Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula Photoperiodic Pathway
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2010 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 186, p. 1033-1044Article in journal (Refereed) Published
Abstract [en]

Perennial plants monitor seasonal changes through changes inenvironmental conditions such as the quantity and quality oflight. To ensure a correct initiation of critical developmentalprocesses, such as the initiation and cessation of growth, plantshave adapted to a spatially variable light regime and genesin the photoperiodic pathway have been implicated as likelysources for these adaptations. Here we examine genetic variationin genes from the photoperiodic pathway in Populus tremula (Salicaceae)for signatures diversifying selection in response to varyinglight regimes across a latitudinal gradient. We fail to identifyany loci with unusually high levels of genetic differentiationamong populations despite identifying four SNPs that show significantallele frequency clines with latitude. We do, however, observelarge covariance in allelic effects across populations for growthcessation, a highly adaptive trait in P. tremula. High covariancein allelic effects is a signature compatible with diversifyingselection along an environmental gradient. We also observe significantlyhigher heterogeneity in genetic differentiation among SNPs fromthe photoperiod genes than among SNPs from randomly chosen genes.This suggests that spatially variable selection could be affectinggenes from the photoperiod pathway even if selection is notstrong enough to cause individual loci to be identified as outliers.SNPs from three genes in the photoperiod pathway (PHYB2, LHY1,and LHY2) show significant associations with natural variationin growth cessation. Collectively these SNPs explain 10–15%of the phenotypic variation in growth cessation. Covariancesin allelic effects across populations help explain an additional5–7% of the phenotypic variation in growth cessation.

Keywords
association study, genetic diversity, populus, bud set
National Category
Genetics Ecology
Identifiers
urn:nbn:se:umu:diva-30358 (URN)10.1534/genetics.110.120873 (DOI)000283996100021 ()2-s2.0-78650974550 (Scopus ID)
Available from: 2009-12-17 Created: 2009-12-17 Last updated: 2023-03-24Bibliographically approved
7. Patterns of selection at the phytochrome A locus in European aspen (Populus tremula)
Open this publication in new window or tab >>Patterns of selection at the phytochrome A locus in European aspen (Populus tremula)
(English)Manuscript (preprint) (Other (popular science, discussion, etc.))
Abstract [en]

When a phenotype with a higher fitness arises in the population the underlying alleles are swept through the population until they reach fixation. The area surrounding the locus of the beneficial allele hitchhikes with the allele under selection, and the size of the area affected depends on the strength of selection. In Populus tremula a < 20kb region on linkage group 13 shows great reduction in synonymous diversity and an increase in rare and derived alleles as indicated by low negative values of Tajima's D and Fay and Wu's H. There is also an increase in associations between allleles at SNP sites in this region. We find that the sweep peaks in exon 2 of the phytochrome A gene. PHYA has not only undergone rapid protein evolution, it also show higher divergence in P. tremula than other plants examined, where it is unusually conserved, further pointing to adaptive significance of the increased rate of protein evolution seen in P. tremula.

Keywords
selective sweep, hitch-hiking, natural selection, nuclotide diversity, populus
National Category
Ecology
Research subject
Genetics
Identifiers
urn:nbn:se:umu:diva-30357 (URN)
Available from: 2009-12-17 Created: 2009-12-17 Last updated: 2018-06-08

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