North Atlantic fucoids in the light of global warming
1. Introduction Distributional changes Acclimation Adaptation Conclusions
North Atlantic fucoids in the light of global
warming
Alexander Jueterbock
Alexander-Jueterbock@web.de
Marine Ecology Research Group
Nord University
Norway
65th Annual meeting of the
British Phycological Society
11-13 Jan 2017
@AJueterbock North Atlantic fucoids in the light of global warming 1 / 57
2. Introduction Distributional changes Acclimation Adaptation Conclusions
Contributors
Galice Hoarau
Irina Smolina
Jorge Fernandes
James A. Coyer
Spyros Kollias
Jeanine L. Olsen
Heroen Verbruggen Lennert Tyberghein
Havkyst projects: 196505, 203839, 216484
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3. Introduction Distributional changes Acclimation Adaptation Conclusions
CO2 increase since the industrial revolution
@AJueterbock North Atlantic fucoids in the light of global warming 3 / 57
4. Introduction Distributional changes Acclimation Adaptation Conclusions
Recent land and ocean warming
Christiansen, J., 2013, Scientific American
@AJueterbock North Atlantic fucoids in the light of global warming 4 / 57
5. Introduction Distributional changes Acclimation Adaptation Conclusions
Climate change responses
..
Temperature
rise
.
Heat waves
.
Seasonality
shi
.
Ocean
acidifica on
.
Migra on
.
Acclima on
.
Adapta on
.
Species
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6. Introduction Distributional changes Acclimation Adaptation Conclusions
High sensitivity of intertidal species
@AJueterbock North Atlantic fucoids in the light of global warming 6 / 57
8. Introduction Distributional changes Acclimation Adaptation Conclusions
Carbon sequestration of 173 TgC yr-1
@AJueterbock North Atlantic fucoids in the light of global warming 7 / 57
9. Introduction Distributional changes Acclimation Adaptation Conclusions
Carbon sequestration of 173 TgC yr-1
Krause-Jensen and Duarte, 2016, Nature Geoscience
@AJueterbock North Atlantic fucoids in the light of global warming 7 / 57
10. Introduction Distributional changes Acclimation Adaptation Conclusions
Temperate seaweed distribution limited by the
10 summer and the 20 winter isotherm
@AJueterbock North Atlantic fucoids in the light of global warming 8 / 57
11. Introduction Distributional changes Acclimation Adaptation Conclusions
Predicting seaweed range shifts under climate change
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Predominant seaweeds in the North-Atlantic
Temperate Arctic
Fucus serratus Fucus
vesiculosus
Ascophyllum
nodosum
Fucus distichus
Shores with biggest ecological change?
@AJueterbock North Atlantic fucoids in the light of global warming 9 / 57
12. Introduction Distributional changes Acclimation Adaptation Conclusions
Ecological Niche Modeling
Present-day conditions
Bio-ORACLE database
Tyberghein et al., 2012, Global Ecology and Biogeography.
Georeferenced Occurrences
DA (m−1)
SST ( )
SAT ( )
Ecological Niche Model (Maxent Phillips et al., 2006, Ecological Modelling)
2000 2100 ? 2200 ?
@AJueterbock North Atlantic fucoids in the light of global warming 10 / 57
13. Introduction Distributional changes Acclimation Adaptation Conclusions
Range-limiting factors
Species Range-limiting factors
TEMPERATEREGIONARCTICREGION
Fucus serratus
Fucus vesiculosus
Ascophyllum nodosum
Fucus distichus
MinimumSST(°C)MeanSST(°C)MaximumSST(°C)MeanSAT(°C)
Min.Diff.Atten.(m−1
)MeanSalinity(PSU)MeanNitrate(µmoll−1
)Min.Chlorophyll(mg/m3
)MeanCalcite(mol/m3
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14. Introduction Distributional changes Acclimation Adaptation Conclusions
Ecological Niche Modeling
Present-day conditions
Bio-ORACLE database
Tyberghein et al., 2012, Global Ecology and Biogeography.
Georeferenced Occurrences
DA (m−1)
SST ( )
SAT ( )
Ecological Niche Model (Maxent Phillips et al., 2006, Ecological Modelling)
2000 2100 ? 2200 ?
CO2 emission scenario changes
SST ( )
SAT ( )
SST ( )
SAT ( )
@AJueterbock North Atlantic fucoids in the light of global warming 12 / 57
15. Introduction Distributional changes Acclimation Adaptation Conclusions
Predicted Niche Shifts until 2200
Based on the intermediate IPCC scenario A1B
Fucus serratus Fucus vesiculosus Ascophyllum nodosum
Fucus distichus
Jueterbock et al., 2013, Ecology and Evolution; Jueterbock et al., 2016, Ecology and Evolution
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16. Introduction Distributional changes Acclimation Adaptation Conclusions
Conclusions from prediced niche shifts
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Biggest ecological change in
Arctic and warm temperate areas
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17. Introduction Distributional changes Acclimation Adaptation Conclusions
Conclusions from prediced niche shifts
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Biggest ecological change in
Arctic and warm temperate areas
Increasing diversity of intertidal
fucoids
Hybridization
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18. Introduction Distributional changes Acclimation Adaptation Conclusions
Hybrid zones of Fucus serratus and Fucus distichus
Hybridization and introgression decreased with increasing duration
of sympatry due to gametic incompatibility
Hoarau et al., 2015, Royal Society Open Science
@AJueterbock North Atlantic fucoids in the light of global warming 15 / 57
19. Introduction Distributional changes Acclimation Adaptation Conclusions
Conclusions from prediced niche shifts
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Biggest ecological change in
Arctic and warm temperate areas
Habitat loss predicted also for subtidal
kelp species
Laminaria digitata and L. hyperborea
Assis et al., 2016, Marine Environmental Research;
Raybaud et al., 2013, PLOS ONE
@AJueterbock North Atlantic fucoids in the light of global warming 16 / 57
20. Introduction Distributional changes Acclimation Adaptation Conclusions
Loss of canopy-forming seaweeds in
warm-temperate regions
Brodie et al., 2014, Ecology and Evolution
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21. Introduction Distributional changes Acclimation Adaptation Conclusions
Integrative niche modeling
Future
distribution
Niche modeling
Phenotypic
plasticity
Adaptation
Dispersal
Biotic
interactions
Eco- evolutionary responding potential
Present-day occurrence
Heat shock response Outlier loci
Occurrence records Environmental conditions
Stable realized niche
Niche shift/evolution
Mitigation of habitat-loss
Increased invasive potential
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22. Introduction Distributional changes Acclimation Adaptation Conclusions
Integrative niche modeling
Future
distribution
Niche modeling
Phenotypic
plasticity
Adaptation
Dispersal
Biotic
interactions
Eco- evolutionary responding potential
Present-day occurrence
Heat shock response Outlier loci
Occurrence records Environmental conditions
Stable realized niche
Niche shift/evolution
Mitigation of habitat-loss
Increased invasive potential
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23. Introduction Distributional changes Acclimation Adaptation Conclusions
Model resolution too low to identify upwelling regions
Lourenço et al., 2016, Journal of Biogeography
Upwelling regions along shores of
SW-Iberia and NW-Africa are
climate change refugia for
F. guiryi
Lourenço et al., 2016, Journal of Biogeography.
@AJueterbock North Atlantic fucoids in the light of global warming 19 / 57
24. Introduction Distributional changes Acclimation Adaptation Conclusions
Integrative niche modeling
Future
distribution
Niche modeling
Phenotypic
plasticity
Adaptation
Dispersal
Biotic
interactions
Eco- evolutionary responding potential
Present-day occurrence
Heat shock response Outlier loci
Occurrence records Environmental conditions
Stable realized niche
Niche shift/evolution
Mitigation of habitat-loss
Increased invasive potential
@AJueterbock North Atlantic fucoids in the light of global warming 20 / 57
25. Introduction Distributional changes Acclimation Adaptation Conclusions
Biotic interactions
Increasing mussel recruitment due to rising sea temperatures
replaces rockweed (A. nodosum) beds in Canada
Ugarte et al., 2009, Journal of Applied Phycology
@AJueterbock North Atlantic fucoids in the light of global warming 21 / 57
26. Introduction Distributional changes Acclimation Adaptation Conclusions
Integrative niche modeling
Future
distribution
Niche modeling
Phenotypic
plasticity
Adaptation
Dispersal
Biotic
interactions
Eco- evolutionary responding potential
Present-day occurrence
Heat shock response Outlier loci
Occurrence records Environmental conditions
Stable realized niche
Niche shift/evolution
Mitigation of habitat-loss
Increased invasive potential
@AJueterbock North Atlantic fucoids in the light of global warming 22 / 57
27. Introduction Distributional changes Acclimation Adaptation Conclusions
Dispersal and invasive potential
Zygote dispersal: <10m
Flotation vesicles
Fucus vesiculosus
Ascophyllum nodosum
low invasive potential
Shipping transport
Fucus serratus
@AJueterbock North Atlantic fucoids in the light of global warming 23 / 57
28. Introduction Distributional changes Acclimation Adaptation Conclusions
Integrative niche modeling
Future
distribution
Niche modeling
Phenotypic
plasticity
Adaptation
Dispersal
Biotic
interactions
Eco- evolutionary responding potential
Present-day occurrence
Heat shock response Outlier loci
Occurrence records Environmental conditions
Stable realized niche
Niche shift/evolution
Mitigation of habitat-loss
Increased invasive potential
@AJueterbock North Atlantic fucoids in the light of global warming 24 / 57
29. Introduction Distributional changes Acclimation Adaptation Conclusions
Dark period
Poleward shift of Laminaria hyperborea in progress
Müller et al., 2009, Botanica Marina
Recent records
Hiscock, K.
@AJueterbock North Atlantic fucoids in the light of global warming 25 / 57
30. Introduction Distributional changes Acclimation Adaptation Conclusions
Integrative niche modeling
Future
distribution
Niche modeling
Phenotypic
plasticity
Adaptation
Dispersal
Biotic
interactions
Eco- evolutionary responding potential
Present-day occurrence
Heat shock response Outlier loci
Occurrence records Environmental conditions
Stable realized niche
Niche shift/evolution
Mitigation of habitat-loss
Increased invasive potential
@AJueterbock North Atlantic fucoids in the light of global warming 26 / 57
31. Introduction Distributional changes Acclimation Adaptation Conclusions
Acclimation potential of Fucus serratus
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Local thermal adaptation?
Areas under highest extinction risk?
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32. Introduction Distributional changes Acclimation Adaptation Conclusions
Common-garden heat stress experiments
Norway
Denmark
Brittany
Spain
@AJueterbock North Atlantic fucoids in the light of global warming 28 / 57
33. Introduction Distributional changes Acclimation Adaptation Conclusions
Common-garden heat stress experiments
Norway
Denmark
Brittany
Spain
Bodø
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34. Introduction Distributional changes Acclimation Adaptation Conclusions
Common-garden heat stress experiments
Norway
Denmark
Brittany
Spain
Bodø
Acclimation at 9
@AJueterbock North Atlantic fucoids in the light of global warming 28 / 57
35. Introduction Distributional changes Acclimation Adaptation Conclusions
Common garden heat stress experiments
Heat stress, 6 ind./pop
Measurements
Photosynthetic performance
hsp gene expression (hsp70, hsp90, shsp)
1h Stress 24h Recovery
9
20
24
28
32
36
T ()
Time
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36. Introduction Distributional changes Acclimation Adaptation Conclusions
Photosynthetic performance
0 4 8 12 16 20 24 28 32 36
Norway
Denmark
Brittany
Spain
Thermal range in year 2200
Measured response
Jueterbock et al., 2014, Marine Genomics
@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57
37. Introduction Distributional changes Acclimation Adaptation Conclusions
Photosynthetic performance
0 4 8 12 16 20 24 28 32 36
Norway
Denmark
Brittany
Spain
Thermal range in year 2200
Measured response
1
Jueterbock et al., 2014, Marine Genomics
@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57
38. Introduction Distributional changes Acclimation Adaptation Conclusions
Photosynthetic performance
0 4 8 12 16 20 24 28 32 36
Norway
Denmark
Brittany
Spain
Thermal range in year 2200
Measured response
1
1. Performance
in 2200
Jueterbock et al., 2014, Marine Genomics
@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57
39. Introduction Distributional changes Acclimation Adaptation Conclusions
Photosynthetic performance
0 4 8 12 16 20 24 28 32 36
Norway
Denmark
Brittany
Spain
Thermal range in year 2200
Measured response
1
1. Performance
in 2200
2
2. Resilience
Jueterbock et al., 2014, Marine Genomics
@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57
40. Introduction Distributional changes Acclimation Adaptation Conclusions
Heat shock response
Constitutive shsp gene expression before heat shock
23 weeks acclimation
7 weeks acclimation
Normalizedexpression
High constitutive
stress
Norway
Denmark
Brittany
Spain
Jueterbock et al., 2014, Marine Genomics
@AJueterbock North Atlantic fucoids in the light of global warming 31 / 57
41. Introduction Distributional changes Acclimation Adaptation Conclusions
Heat shock response
Constitutive shsp gene expression before heat shock
23 weeks acclimation
7 weeks acclimation
Normalizedexpression
High constitutive
stress
Norway
Denmark
Brittany
Spain
Heat shock response of shsp gene expression after 24h recovery
Foldchange
Reduced
responsiveness
Norway
Denmark
Brittany
Spain
Jueterbock et al., 2014, Marine Genomics
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42. Introduction Distributional changes Acclimation Adaptation Conclusions
Conclusions
Acclimation
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Local thermal adaptation
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43. Introduction Distributional changes Acclimation Adaptation Conclusions
Acclimation potential of Fucus distichus
Responsiveness also reduced towards the south
Smolina et al., 2016, Royal Society Open Science
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44. Introduction Distributional changes Acclimation Adaptation Conclusions
Conclusions
Acclimation
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Areas under highest extinction risk?
Brittany and Spain
Confirms predicted habitat loss
Jueterbock et al., 2013, Ecology
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47. Introduction Distributional changes Acclimation Adaptation Conclusions
Threatened refugial populations
Ice cover during the Last Glacial Maximum (18-20 kya)
@AJueterbock North Atlantic fucoids in the light of global warming 36 / 57
48. Introduction Distributional changes Acclimation Adaptation Conclusions
Genetically diverse refugia under threat
Fucus serratus
Glacial refugia identified by mtDNA haplotype diversity
Hoarau et al., 2007, Molecular Ecology Notes
@AJueterbock North Atlantic fucoids in the light of global warming 37 / 57
49. Introduction Distributional changes Acclimation Adaptation Conclusions
1,250 km northward shift of Fucus vesiculosus
and loss of distinct genetic variation
Nicastro et al., 2013, BMC Biology
Loss of southern lineages means
loss of increased heat stress
tolerance
Saada et al., 2016, Diversity and Distributions
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50. Introduction Distributional changes Acclimation Adaptation Conclusions
Genetic diversity increases stress tolerance
Low diversity decreases survival in Fucus vesiculosus offspring
adjusted from Al-Janabi et al., 2016, Marine Biology
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51. Introduction Distributional changes Acclimation Adaptation Conclusions
Remaining key question
Can ancient refugial populations
adapt to climate change
or
will temperate seaweeds
lose their centers of genetic diversity?
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52. Introduction Distributional changes Acclimation Adaptation Conclusions
Adaptation
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Effective population size Ne? Genetic changes (past 10 yrs)?
@AJueterbock North Atlantic fucoids in the light of global warming 41 / 57
53. Introduction Distributional changes Acclimation Adaptation Conclusions
Sampling scheme (50–75 ind./pop)
∼ 2000 ∼ 2010
Spatial(environmental)effects
Temporal changes
1 decade
of selection
@AJueterbock North Atlantic fucoids in the light of global warming 42 / 57
54. Introduction Distributional changes Acclimation Adaptation Conclusions
Methods and analysis
∼ 2000 ∼ 2010
Spatial(environmental)effects
Temporal changes
1 decade
of selection
Genotyping
31 microsatellite markers (20 EST-linked)
Analysis
Effective population size (Ne)
Allelic richness (α)
Temporal outlier loci
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55. Introduction Distributional changes Acclimation Adaptation Conclusions
Methods and analysis
∼ 2000 ∼ 2010
Spatial(environmental)effects
Temporal changes
1 decade
of selection
Genotyping
31 microsatellite markers (20 EST-linked)
Analysis
Effective population size (Ne)
Allelic richness (α)
Temporal outlier loci
@AJueterbock North Atlantic fucoids in the light of global warming 44 / 57
56. Introduction Distributional changes Acclimation Adaptation Conclusions
Effective population size Ne
Reflecting adaptive capacity
∼ 2000 ∼ 2010
18
63
207
23
Norway
Denmark
Brittany
Spain
32
61
210
26
Estimates excluding outlier loci
Jueterbock, 2013
@AJueterbock North Atlantic fucoids in the light of global warming 45 / 57
57. Introduction Distributional changes Acclimation Adaptation Conclusions
Methods
∼ 2000 ∼ 2010
Spatial(environmental)effects
Temporal changes
1 decade
of selection
Genotyping
31 microsatellite markers (20 EST-linked)
Analysis
Effective population size (Ne)
Allelic richness (α)
Temporal outlier loci
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58. Introduction Distributional changes Acclimation Adaptation Conclusions
Changes in allelic richness
∼ 2000 ∼ 2010
3.1
4.6
8.0
4.0
Norway
Denmark
Brittany
Spain
3.3
4.8
7.9
4.6
Significant
decline
Jueterbock, 2013
@AJueterbock North Atlantic fucoids in the light of global warming 47 / 57
59. Introduction Distributional changes Acclimation Adaptation Conclusions
Methods
∼ 2000 ∼ 2010
Spatial(environmental)effects
Temporal changes
1 decade
of selection
Genotyping
31 microsatellite markers (20 EST-linked)
Analysis
Effective population size (Ne)
Allelic richness (α)
Genetic differentiation (Dest)
Temporal outlier loci
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60. Introduction Distributional changes Acclimation Adaptation Conclusions
Outlier loci
Temporal outlier loci
0%
6%
23%
13%
Norway
Denmark
Brittany
Spain
Strongest selection pressure in the South
Adaptive to climate change?
Jueterbock, 2013
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61. Introduction Distributional changes Acclimation Adaptation Conclusions
Conclusions
Adaptation
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Adaptive responsiveness
highest in Brittany
and likely insufficient in Spain
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62. Introduction Distributional changes Acclimation Adaptation Conclusions
Brown algal genome sequencing projects
De novo Fucus vesiculosus genome, part of IMAGO Marine
Genome project (University of Gothenburg, Sweden)
Sequencing of some 30 brown algal genomes, including Fucus
spp. (Roscoff Research Station, France)
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63. Introduction Distributional changes Acclimation Adaptation Conclusions
Remaining questions and future directions
Can microbiome and epigenetic variation contribute to rapid
adaptation?
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64. Introduction Distributional changes Acclimation Adaptation Conclusions
Adaptive role of the seaweed microbiome
Microorganisms
provide functions related to host health and defense
facilitated acclimation of Ectocarpus to fresh water (Dittami
et al., 2015)
Egan et al., 2013, FEMS microbiology reviews
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65. Introduction Distributional changes Acclimation Adaptation Conclusions
Epigenetic modifications add
a level of variation to the genome
Allis et al., 2015
@AJueterbock North Atlantic fucoids in the light of global warming 54 / 57
66. Introduction Distributional changes Acclimation Adaptation Conclusions
Compensation for absence of genetic variation
DNA-methylation variation increased productivity and stability in
Arabidoposis thaliana
Latzel et al., 2013, Nature communications
Unclear if DNA-methylation exists in brown algae
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67. Introduction Distributional changes Acclimation Adaptation Conclusions
Summary
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Highest responsiveness
in Brittany
Adaptive value remains unknown
Seaweed meadows:
Loss in warm-
temperate regions
Arctic invasion?
Ancient refugia
under threat:
stress in Brittany
Extinction risk in Spain
@AJueterbock North Atlantic fucoids in the light of global warming 56 / 57
68. Introduction Distributional changes Acclimation Adaptation Conclusions
Remaining key questions
Adaptation or acclimation to Arctic dark periods?
Adaptation or extinction in genetically diverse ancient glacial
refugia?
Role of epigenetics and microbiome for rapid adaptation?
@AJueterbock North Atlantic fucoids in the light of global warming 57 / 57
69. References
References I
Allis, CD, ML Caparros, T Jenuwein, and D Reinberg (2015).
Epigenetics. P. 984.
Assis, J, AV Lucas, I Bárbara, and EÁ Serrão (2016). “Future
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Brodie, J, CJ Williamson, Da Smale, Na Kamenos,
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70. References
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Dittami, SM, L Duboscq-Bidot, M Perennou, A Gobet, E Corre,
C Boyen, et al. (2015). “Host-microbe interactions as a driver of
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Egan, S, T Harder, C Burke, P Steinberg, S Kjelleberg, T Thomas,
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seaweed-bacteria interactions.” In: FEMS microbiology reviews
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71. References
References III
Hansen, MM, EE Nielsen, and KLD Mensberg (2006).
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Harley, CDG, KM Anderson, KW Demes, JP Jorve, RL Kordas,
TA Coyle, et al. (2012). “Effects of climate change on global
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Hoarau, G, JA Coyer, M Giesbers, A Jueterbock, and JL Olsen
(2015). “Pre-zygotic isolation in the macroalgal genus Fucus
from four contact zones spanning 100–10 000 years: a tale of
reinforcement?” In: Royal Society Open Science 2.2, p. 140538.
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Hoarau, G, J Coyer, WT Stam, and JL Olsen (2007). “A fast and
inexpensive DNA extraction/purification protocol for brown
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Al-Janabi, B, I Kruse, A Graiff, U Karsten, and M Wahl (2016).
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textit{Fucus serratus}, a key foundational species on North
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@AJueterbock North Atlantic fucoids in the light of global warming 4 / 11
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References V
Jueterbock, A, S Kollias, I Smolina, JMO Fernandes, JA Coyer,
JL Olsen, et al. (2014). “Thermal stress resistance of the brown
alga textit{Fucus serratus} along the North-Atlantic coast:
Acclimatization potential to climate change.” In: Marine
Genomics 13, pp. 27–36.
Jueterbock, A, L Tyberghein, H Verbruggen, JA Coyer, JL Olsen,
and G Hoarau (2013). “Climate change impact on seaweed
meadow distribution in the {North Atlantic} rocky intertidal.”
In: Ecology and Evolution 3.5, pp. 1356–1373.
Jueterbock, A, I Smolina, JA Coyer, and G Hoarau (2016). “The
fate of the Arctic seaweed Fucus distichus under climate change:
an ecological niche modeling approach.” In: Ecology and
Evolution, n/a–n/a.
@AJueterbock North Atlantic fucoids in the light of global warming 5 / 11
74. References
References VI
Krause-Jensen, D and CM Duarte (2016). “Substantial role of
macroalgae in marine carbon sequestration.” In: Nature
Geoscience 9.10, pp. 737–742.
Latzel, V, E Allan, A Bortolini Silveira, V Colot, M Fischer, and
O Bossdorf (2013). “Epigenetic diversity increases the
productivity and stability of plant populations.” In: Nature
communications 4, p. 2875.
Lourenço, CR, GI Zardi, CD McQuaid, Ea Serrão, Ga Pearson,
R Jacinto, et al. (2016). “Upwelling areas as climate change
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Temporal outlier loci indicate selective sweeps
Before Selection After Selection
Selective Sweep
based on Vitti et al., 2012, Trends in Genetics
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