Oral presentation in 2015 at the 53rd Annual Northeast Algal Symposium ‘Algae as model systems’, Salve Regina University, Newport, United States

1. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Seaweed in the light of global climate change
Alexander Jueterbock
Alexander-Jueterbock@web.de
Marine Ecology Research Group
Faculty of Biosciences and Aquaculture
University of Nordland
Norway
53rd NEAS Symposium
Algae as Model Systems
27.04.2014
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2. Introduction Distributional changes Acclimation Adaptation Overall 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 Overall conclusions
CO2 increase since the industrial revolution
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4. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Recent land and ocean warming
Christiansen, J.; Scientific American (2013)
4 / 60

5. Introduction Distributional changes Acclimation Adaptation Overall 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 Overall conclusions
High sensitivity of intertidal species
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7. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Seaweeds as model systems
to investigate climate change
Seaweeds provide an excellent system to investigate climate change
impact
Intertidal key species
Distribution directly limited by temperature tolerance
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8. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Seaweeds are key species in temperate
North Atlantic regions
© Hoarau, G., 2010
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9. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Seaweeds are key species in temperate
North Atlantic regions
8 / 60

10. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Seaweeds as model systems
to investigate climate change
Seaweeds provide an excellent system to investigate climate change
impact
Intertidal key species
Distribution directly limited by temperature tolerance
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11. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Temperate seaweed distribution limited by the
10 summer and the 20 winter isotherm
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12. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Seaweeds as model systems
to investigate climate change
Seaweeds provide an excellent system to investigate climate change
impact
Intertidal key species
Distribution directly limited by temperature tolerance
Range shifts of seaweeds in response to SST-shifts can
trigger major ecological changes
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13. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Recent warming in the North Atlantic
Shift of the 15°C isotherm
330 km north
1985 2000
[McMahon & Hays, 2006; Global Change Biol.]
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14. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Predicted northward shift of SST isotherms
Poleward migration of SST isotherms under
IPCC scenario A2 until 2100:
30-90 km/decade along North Atlantic shores
[Hansen et al., 2006; PNAS]
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15. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Predicting seaweed range shifts under climate change
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Predominant seaweeds in the North-Atlantic
Fucus serratus Fucus
vesiculosus
Ascophyllum
nodosum
Shores with biggest ecological change?
Assemblage shift?
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16. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Ecological Niche Modeling
Present-day conditions
Bio-ORACLE database
[Tyberghein et al., 2011; Global Ecol. Biogeogr.].
Georeferenced Occurrences
DA (m−1)
SST ( )
SAT ( )
Ecological Niche Model (Maxent [Phillips et al., 2006; Ecol. Model.])
2000 2100 ? 2200 ?
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17. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Ecological Niche Modeling
Present-day conditions
Bio-ORACLE database
[Tyberghein et al., 2011; Global Ecol. Biogeogr.].
Georeferenced Occurrences
DA (m−1)
SST ( )
SAT ( )
Ecological Niche Model (Maxent [Phillips et al., 2006; Ecol. Model.])
2000 2100 ? 2200 ?
CO2 emission scenario changes
SST ( )
SAT ( )
SST ( )
SAT ( )
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18. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Predicted Niche Shifts
Based on the intermediate IPCC scenario A1B
[Jueterbock et al., 2013; Ecol. Evol.]
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19. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Predicted Niche Shifts
Based on the intermediate IPCC scenario A1B
Habitat gain in the Arctic
[Jueterbock et al., 2013; Ecol. Evol.]
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20. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Predicted Niche Shifts
Based on the intermediate IPCC scenario A1B
Habitat loss in warm temperate areas
[Jueterbock et al., 2013; Ecol. Evol.]
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21. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Predominant seaweeds shift northward as an
assemblage
West-Atlantic East-Atlantic
F. serratus F. vesiculosus A. nodosum
[Jueterbock et al., 2013; Ecol. Evol.]
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22. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Conclusions from prediced niche shifts
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Biggest ecological change in
warm temperate and Arctic areas
Assemblage shift
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23. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Conclusions from prediced niche shifts
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Biggest ecological change in
warm temperate and Arctic areas
Assemblage shift
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24. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Colonization of Arctic shores
The poleward shift of temperate intertidal seaweeds depends on
three key factors
Dispersal and invasive potential
Dark period
Competitive interactions
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25. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Colonization of Arctic shores
The poleward shift of temperate intertidal seaweeds depends on
three key factors
Dispersal and invasive potential
Dark period
Competitive interactions
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26. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Dispersal and invasive potential
Low dispersal of juvenile stages in fucoid algae
[Braune, 2008; Meeresalgen]
♂ ♀ dioecious
zygote dispersal: <10m
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27. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Dispersal and invasive potential
Flotation vesicles
Fucus vesiculosus
Ascophyllum nodosum
low invasive potential
Shipping transport
Fucus serratus
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28. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Dispersal and invasive potential
Shipping transport introduced F. serratus to Canada
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29. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Colonization of Arctic shores
The poleward shift of temperate intertidal seaweeds depends on
three key factors
Dispersal and invasive potential
Dark period
Competitive interactions
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30. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Dark period
Poleward shift of Laminaria hyperborea in progress
[Müller et al., 2009; Bot. Mar.]
Recent records
Hiscock, K.
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31. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Colonization of Arctic shores
The poleward shift of temperate intertidal seaweeds depends on
three key factors
Dispersal and invasive potential
Dark period
Competitive interactions
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32. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Competitive interactions
Fucus distichus predominates the Arctic intertidal
Habitat suitability of
F. distichus
based on ENM [Smolina, I., 2012]
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33. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Competitive interactions
[Smolina, I., 2012]
Increase of sympatry
zones/hybridization
Competition
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34. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Conclusions from prediced niche shifts
..
Migra on
.
Acclima on
.
Adapta on
.Inter dal
seaweed
Biggest ecological change in
warm temperate and Arctic areas
Assemblage shift
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35. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Climate change impact also on subtidal kelp
[Raybaud et al., 2013; PLOS ONE]
Percentage of models forecasting a
disappearance of Laminaria digitata
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36. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Ecological Niche Models neglect biotic interactions
Ecological Niche Models do not take
biotic interactions into account
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37. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Biotic interactions
Increasing mussel recruitment due to rising sea temperatures
replaces rockweed (A. nodosum) beds in Canada
[Ugarte, 2009; J. Appl. Phycol.]
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38. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Biotic interactions
Grazing pressure
[Harley et al., 2012; J. Phycol]
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39. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Biotic interactions
Grazing pressure
[Harley et al., 2012; J. Phycol]
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40. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Ecological Niche Models neglect species responses
Ecological Niche Models do not take
the plastic or adaptive potential
of species into account
..
Migra on
.
Acclima on
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Adapta on
.Inter dal
seaweed
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41. Introduction Distributional changes Acclimation Adaptation Overall 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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42. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Common-garden heat stress experiments
Norway
Denmark
Brittany
Spain
34 / 60

43. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Common-garden heat stress experiments
Norway
Denmark
Brittany
Spain
Bodø
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44. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Common-garden heat stress experiments
Norway
Denmark
Brittany
Spain
Bodø
Acclimation at 9
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45. Introduction Distributional changes Acclimation Adaptation Overall 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 (°C)
Time
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46. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Photosynthetic performance
0 4 8 12 16 20 24 28 32 36
Measured response
[Jueterbock et al., 2014; Mar. Genomics]
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47. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Photosynthetic performance
0 4 8 12 16 20 24 28 32 36
Measured response
1
[Jueterbock et al., 2014; Mar. Genomics]
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48. Introduction Distributional changes Acclimation Adaptation Overall 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; Mar. Genomics]
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49. Introduction Distributional changes Acclimation Adaptation Overall 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; Mar. Genomics]
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50. Introduction Distributional changes Acclimation Adaptation Overall 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; Mar. Genomics]
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51. Introduction Distributional changes Acclimation Adaptation Overall 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; Mar. Genomics]
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52. Introduction Distributional changes Acclimation Adaptation Overall 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; Mar. Genomics]
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53. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Conclusions
Acclimation
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Local thermal adaptation
Areas under highest extinction risk?
Brittany and Spain
Confirms predicted habitat loss
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54. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Ribadeo, Spain © Coyer, J.A., 1999
[Jueterbock et al., 2013; Ecol. Evol., Fig. S6]
1999: extensive F. serratus meadows
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55. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Ribadeo, Spain © Jueterbock, A., 2010
[Jueterbock et al., 2013; Ecol. Evol., Fig. S6]
90% abundance decline in 11 years
[Viejo et al., 2011; Ecography]
Dwarf forms with
reduced reproductive
capacity in Spain
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56. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Threatened refugial populations
Ice cover during the Last Glacial Maximum (18-20 kya)
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57. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Genetically diverse refugia under threat
Fucus serratus
Glacial refugia identified by mtDNA haplotype diversity
[Hoarau et al., 2007; Mol. Ecol.]
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58. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Genetically diverse refugia under threat
Fucus serratus
[Hoarau et al., 2007; Mol. Ecol.]
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59. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Genetically diverse refugia under threat
Chondrus crispus
Based on mitochondrial SNPs
[Provan & Maggs, 2012; Proc. R. Soc. London, Ser. B]
180 km retreat since 1971
from a Portuguese refugium
Interglacial distribution
Glacial distribution
Stable refugium
under threat
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60. Introduction Distributional changes Acclimation Adaptation Overall 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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61. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Adaptation
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Effective population size Ne? Genetic changes (past 10 yrs)?
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62. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Sampling scheme (50–75 ind./pop)
∼ 2000 ∼ 2010
Spatial(environmental)effects
Temporal changes
1 decade
of selection
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63. Introduction Distributional changes Acclimation Adaptation Overall 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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64. Introduction Distributional changes Acclimation Adaptation Overall 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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65. Introduction Distributional changes Acclimation Adaptation Overall 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; PhD Thesis]
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66. Introduction Distributional changes Acclimation Adaptation Overall 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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67. Introduction Distributional changes Acclimation Adaptation Overall 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; PhD Thesis]
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68. Introduction Distributional changes Acclimation Adaptation Overall 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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69. Introduction Distributional changes Acclimation Adaptation Overall conclusions
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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70. Introduction Distributional changes Acclimation Adaptation Overall 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; PhD Thesis]
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71. Introduction Distributional changes Acclimation Adaptation Overall 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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72. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Fucus in the tree of life
distantly related to other taxa
The genome of Ectocarpus siliculosus is sequenced but Fucales
and Ectocarpales diverged in the Cretaceous (ca. 125 Ma)
[Cock et al., 2010; Nature]
De novo Fucus vesiculosus genome until 2017, part of IMAGO
Marine Genome project (University of Gothenburg, Sweden)
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73. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Summary
..
Migra on
.
Acclima on
.
Adapta on
.Fucus
serratus
Highest responsiveness
in Brittany
Adaptive value re-
mains unknown
Seaweed meadows:
Loss in warm-
temperate regions
Arctic invasion?
Ancient refugia
under threat:
stress in Brittany
Extinction risk in Spain
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74. Introduction Distributional changes Acclimation Adaptation Overall 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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75. Introduction Distributional changes Acclimation Adaptation Overall conclusions
Overall conclusion
Seaweeds as model systems to investigate climate change
Seaweeds provide an excellent system to investigate climate change
impact on North Atlantic rocky shores
Intertidal key species
Distribution directly limited by temperature tolerance
Annotated genome of Fucus sp. needed (IMAGO)
Remaining key question: Adaptation or extinction in genetically
diverse ancient glacial refugia?
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76. Introduction Distributional changes Acclimation Adaptation Overall conclusions
60 / 60

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