Introduction Distributional changes Acclimation Adaptation Conclusions

North Atlantic fucoids in the light of globalwarming

Alexander JueterbockAlexander-Jueterbock@web.de

Marine Ecology Research GroupNord University

Norway

65th Annual meeting of theBritish Phycological Society

11-13 Jan 2017

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Introduction Distributional changes Acclimation Adaptation Conclusions

Contributors

Galice Hoarau

Irina Smolina

Jorge Fernandes

James A. Coyer

Spyros Kollias

Jeanine L. Olsen

Heroen Verbruggen Lennert TybergheinHavkyst projects: 196505, 203839, 216484

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Introduction Distributional changes Acclimation Adaptation Conclusions

CO2 increase since the industrial revolution

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Introduction Distributional changes Acclimation Adaptation Conclusions

Recent land and ocean warming

Christiansen, J., 2013, Scientific American

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Introduction Distributional changes Acclimation Adaptation Conclusions

Climate change responses

..

Temperaturerise

.

Heat waves

.

Seasonalityshi

.

Oceanacidifica on

.

Migra on

.

Acclima on

.

Adapta on

.Species

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Introduction Distributional changes Acclimation Adaptation Conclusions

High sensitivity of intertidal species

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Introduction Distributional changes Acclimation Adaptation Conclusions

Carbon sequestration of 173 TgC yr-1

© Hoarau, G., 2010

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Introduction Distributional changes Acclimation Adaptation Conclusions

Carbon sequestration of 173 TgC yr-1

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Introduction Distributional changes Acclimation Adaptation Conclusions

Carbon sequestration of 173 TgC yr-1

Krause-Jensen and Duarte, 2016, Nature Geoscience

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Introduction Distributional changes Acclimation Adaptation Conclusions

Temperate seaweed distribution limited by the10℃ summer and the 20℃ winter isotherm

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Introduction Distributional changes Acclimation Adaptation Conclusions

Predicting seaweed range shifts under climate change

..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed

Predominant seaweeds in the North-Atlantic

Temperate Arctic

Fucus serratus Fucusvesiculosus

Ascophyllumnodosum

Fucus distichus

Shores with biggest ecological change?

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Introduction Distributional changes Acclimation Adaptation Conclusions

Ecological Niche Modeling

Present-day conditionsBio-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 ?

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Introduction Distributional changes Acclimation Adaptation Conclusions

Range-limiting factorsSpecies Range-limiting factors

TEMPE

RATE

REGION

ARCT

ICRE

GION

Fucus serratus

Fucus vesiculosus

Ascophyllum nodosum

Fucus distichus

Minim

umSS

T(°

C)

MeanSS

T(°

C)

Maxim

umSS

T(°

C)

MeanSA

T(°

C)

Min.Diff.

Atten.

(m−1 )

MeanSa

linity

(PSU

)MeanNitra

te(µ

moll

−1 )

Min.Ch

lorop

hyll(m

g/m

3 )MeanCa

lcite

(mol/m

3 )@AJueterbock North Atlantic fucoids in the light of global warming 11 / 57

Introduction Distributional changes Acclimation Adaptation Conclusions

Ecological Niche Modeling

Present-day conditionsBio-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 (℃)

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Introduction Distributional changes Acclimation Adaptation Conclusions

Predicted Niche Shifts until 2200Based 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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Introduction Distributional changes Acclimation Adaptation Conclusions

Conclusions from prediced niche shifts

..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed

Biggest ecological change inArctic and warm temperate areas

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Introduction Distributional changes Acclimation Adaptation Conclusions

Conclusions from prediced niche shifts

..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed

Biggest ecological change inArctic and warm temperate areas

Increasing diversity of intertidalfucoids

Hybridization

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Introduction Distributional changes Acclimation Adaptation Conclusions

Hybrid zones of Fucus serratus and Fucus distichusHybridization and introgression decreased with increasing duration

of sympatry due to gametic incompatibility

Hoarau et al., 2015, Royal Society Open Science

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Introduction Distributional changes Acclimation Adaptation Conclusions

Conclusions from prediced niche shifts

..

Migra on

.

Acclima on

.

Adapta on

.Inter dalseaweed

Biggest ecological change inArctic and warm temperate areas

Habitat loss predicted also for subtidalkelp speciesLaminaria digitata and L. hyperboreaAssis et al., 2016, Marine Environmental Research;

Raybaud et al., 2013, PLOS ONE

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Introduction Distributional changes Acclimation Adaptation Conclusions

Loss of canopy-forming seaweeds inwarm-temperate regions

Brodie et al., 2014, Ecology and Evolution

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Introduction Distributional changes Acclimation Adaptation Conclusions

Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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Introduction Distributional changes Acclimation Adaptation Conclusions

Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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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 ofSW-Iberia and NW-Africa areclimate change refugia forF. guiryiLourenço et al., 2016, Journal of Biogeography.

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Introduction Distributional changes Acclimation Adaptation Conclusions

Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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Introduction Distributional changes Acclimation Adaptation Conclusions

Biotic interactionsIncreasing mussel recruitment due to rising sea temperatures

replaces rockweed (A. nodosum) beds in Canada

Ugarte et al., 2009, Journal of Applied Phycology

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Introduction Distributional changes Acclimation Adaptation Conclusions

Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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Introduction Distributional changes Acclimation Adaptation Conclusions

Dispersal and invasive potential

Zygote dispersal: <10m

Flotation vesiclesFucus vesiculosus

Ascophyllum nodosumlow invasive potential

Shipping transport

Fucus serratus

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Introduction Distributional changes Acclimation Adaptation Conclusions

Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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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.

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Introduction Distributional changes Acclimation Adaptation Conclusions

Integrative niche modeling

Futuredistribution

Niche modeling

Phenotypicplasticity

Adaptation

DispersalBiotic

interactions

Eco- evolutionary responding potential

Present-day occurrence

Heat shock response Outlier loci

Occurrence records Environmental conditions

Stable realized niche

Niche shift/evolutionMitigation of habitat-lossIncreased invasive potential

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Introduction Distributional changes Acclimation Adaptation Conclusions

Acclimation potential of Fucus serratus

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Local thermal adaptation?

Areas under highest extinction risk?

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Introduction Distributional changes Acclimation Adaptation Conclusions

Common-garden heat stress experiments

Norway

Denmark

BrittanySpain

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Introduction Distributional changes Acclimation Adaptation Conclusions

Common-garden heat stress experiments

Norway

Denmark

BrittanySpain

Bodø

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Introduction Distributional changes Acclimation Adaptation Conclusions

Common-garden heat stress experiments

Norway

Denmark

BrittanySpain

Bodø

Acclimation at 9℃

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Introduction Distributional changes Acclimation Adaptation Conclusions

Common garden heat stress experiments

Heat stress, > 6 ind./pop

MeasurementsPhotosynthetic performancehsp gene expression (hsp70, hsp90, shsp)

1h Stress 24h Recovery

9℃

20℃24℃28℃32℃36℃

T ()

Time

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Introduction Distributional changes Acclimation Adaptation Conclusions

Photosynthetic performance

0 4 8 12 16 20 24 28 32 36 ℃

NorwayDenmarkBrittanySpain

Thermal range in year 2200

Measured response

1

1. Performancein 2200

2

2. Resilience

Jueterbock et al., 2014, Marine Genomics@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57

Introduction Distributional changes Acclimation Adaptation Conclusions

Photosynthetic performance

0 4 8 12 16 20 24 28 32 36 ℃

NorwayDenmarkBrittanySpain

Thermal range in year 2200

Measured response

1

1. Performancein 2200

2

2. Resilience

Jueterbock et al., 2014, Marine Genomics@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57

Introduction Distributional changes Acclimation Adaptation Conclusions

Photosynthetic performance

0 4 8 12 16 20 24 28 32 36 ℃

NorwayDenmarkBrittanySpain

Thermal range in year 2200

Measured response

1

1. Performancein 2200

2

2. Resilience

Jueterbock et al., 2014, Marine Genomics@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57

Introduction Distributional changes Acclimation Adaptation Conclusions

Photosynthetic performance

0 4 8 12 16 20 24 28 32 36 ℃

NorwayDenmarkBrittanySpain

Thermal range in year 2200

Measured response

1

1. Performancein 2200

2

2. Resilience

Jueterbock et al., 2014, Marine Genomics@AJueterbock North Atlantic fucoids in the light of global warming 30 / 57

Introduction Distributional changes Acclimation Adaptation Conclusions

Heat shock responseConstitutive shsp gene expression before heat shock

23 weeks acclimation

7 weeks acclimation

Normalize

dexpressio

n

High constitutivestress

Norway

DenmarkBrittanySpain

Heat shock response of shsp gene expression after 24h recovery

Fold

change

Reducedresponsiveness

Norway

DenmarkBrittanySpain

Jueterbock et al., 2014, Marine Genomics

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Introduction Distributional changes Acclimation Adaptation Conclusions

Heat shock responseConstitutive shsp gene expression before heat shock

23 weeks acclimation

7 weeks acclimation

Normalize

dexpressio

n

High constitutivestress

Norway

DenmarkBrittanySpain

Heat shock response of shsp gene expression after 24h recovery

Fold

change

Reducedresponsiveness

Norway

DenmarkBrittanySpain

Jueterbock et al., 2014, Marine Genomics

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Introduction Distributional changes Acclimation Adaptation Conclusions

ConclusionsAcclimation

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Local thermal adaptation

Jueterbock et al., 2013, Ecology

and Evolution

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Introduction Distributional changes Acclimation Adaptation Conclusions

Acclimation potential of Fucus distichusResponsiveness also reduced towards the south

Smolina et al., 2016, Royal Society Open Science

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Introduction Distributional changes Acclimation Adaptation Conclusions

ConclusionsAcclimation

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Areas under highest extinction risk?Brittany and Spain

Confirms predicted habitat loss

Jueterbock et al., 2013, Ecology

and Evolution@AJueterbock North Atlantic fucoids in the light of global warming 34 / 57

Introduction Distributional changes Acclimation Adaptation Conclusions

Ribadeo, Spain © Coyer, J.A., 1999Jueterbock2013

1999: extensive F. serratus meadows

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Introduction Distributional changes Acclimation Adaptation Conclusions

Ribadeo, Spain © Jueterbock, A., 2010Jueterbock2013

90% abundance decline in 11 years

Viejo et al., 2011, Ecography

Dwarf forms withreduced reproductivecapacity in Spain

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Introduction Distributional changes Acclimation Adaptation Conclusions

Threatened refugial populations

Ice cover during the Last Glacial Maximum (18-20 kya)

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Introduction Distributional changes Acclimation Adaptation Conclusions

Genetically diverse refugia under threatFucus serratus

Glacial refugia identified by mtDNA haplotype diversityHoarau et al., 2007, Molecular Ecology Notes

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Introduction Distributional changes Acclimation Adaptation Conclusions

1,250 km northward shift of Fucus vesiculosusand loss of distinct genetic variation

Nicastro et al., 2013, BMC Biology

Loss of southern lineages meansloss of increased heat stresstoleranceSaada et al., 2016, Diversity and Distributions

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Introduction Distributional changes Acclimation Adaptation Conclusions

Genetic diversity increases stress tolerance

Low diversity decreases survival in Fucus vesiculosus offspringadjusted from Al-Janabi et al., 2016, Marine Biology

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Introduction Distributional changes Acclimation Adaptation Conclusions

Remaining key question

Can ancient refugial populationsadapt to climate change

orwill temperate seaweeds

lose their centers of genetic diversity?

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Introduction Distributional changes Acclimation Adaptation Conclusions

Adaptation

..

Migra on

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Acclima on

.

Adapta on

.Fucusserratus

Effective population size Ne? Genetic changes (past 10 yrs)?

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Introduction Distributional changes Acclimation Adaptation Conclusions

Sampling scheme (50–75 ind./pop)

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes

1 decadeof selection

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Introduction Distributional changes Acclimation Adaptation Conclusions

Methods and analysis

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes

1 decadeof selection

Genotyping31 microsatellite markers (20 EST-linked)

AnalysisEffective population size (Ne)Allelic richness (α)Temporal outlier loci

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Introduction Distributional changes Acclimation Adaptation Conclusions

Methods and analysis

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes

1 decadeof selection

Genotyping31 microsatellite markers (20 EST-linked)

AnalysisEffective population size (Ne)Allelic richness (α)Temporal outlier loci

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Introduction Distributional changes Acclimation Adaptation Conclusions

Effective population size NeReflecting adaptive capacity

∼ 2000 ∼ 2010

18

6320723

Norway

DenmarkBrittanySpain

32

6121026

Estimates excluding outlier loci

Jueterbock, 2013

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Introduction Distributional changes Acclimation Adaptation Conclusions

Methods

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes

1 decadeof selection

Genotyping31 microsatellite markers (20 EST-linked)

AnalysisEffective population size (Ne)Allelic richness (α)Temporal outlier loci

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Introduction Distributional changes Acclimation Adaptation Conclusions

Changes in allelic richness

∼ 2000 ∼ 2010

3.1

4.68.04.0

Norway

DenmarkBrittanySpain

3.3

4.87.94.6

Significantdecline

Jueterbock, 2013

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Introduction Distributional changes Acclimation Adaptation Conclusions

Methods

∼ 2000 ∼ 2010

Spatial

(enviro

nmental)eff

ects

Temporal changes

1 decadeof selection

Genotyping31 microsatellite markers (20 EST-linked)

AnalysisEffective population size (Ne)Allelic richness (α)Genetic differentiation (Dest)Temporal outlier loci

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Introduction Distributional changes Acclimation Adaptation Conclusions

Outlier loci

Temporal outlier loci

0%

6%23%13%

Norway

DenmarkBrittanySpain

Strongest selection pressure in the SouthAdaptive to climate change?

Jueterbock, 2013

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Introduction Distributional changes Acclimation Adaptation Conclusions

ConclusionsAdaptation

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Adaptive responsivenesshighest in Brittany

and likely insufficient in Spain

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Introduction Distributional changes Acclimation Adaptation Conclusions

Brown algal genome sequencing projects

De novo Fucus vesiculosus genome, part of IMAGO MarineGenome project (University of Gothenburg, Sweden)Sequencing of some 30 brown algal genomes, including Fucusspp. (Roscoff Research Station, France)

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Introduction Distributional changes Acclimation Adaptation Conclusions

Remaining questions and future directions

Can microbiome and epigenetic variation contribute to rapidadaptation?

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Introduction Distributional changes Acclimation Adaptation Conclusions

Adaptive role of the seaweed microbiomeMicroorganisms

provide functions related to host health and defensefacilitated acclimation of Ectocarpus to fresh water (Dittamiet al., 2015)

Egan et al., 2013, FEMS microbiology reviews

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Introduction Distributional changes Acclimation Adaptation Conclusions

Epigenetic modifications adda level of variation to the genome

Allis et al., 2015

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Introduction Distributional changes Acclimation Adaptation Conclusions

Compensation for absence of genetic variation

DNA-methylation variation increased productivity and stability inArabidoposis thaliana

Latzel et al., 2013, Nature communications

Unclear if DNA-methylation exists in brown algae

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Introduction Distributional changes Acclimation Adaptation Conclusions

Summary

..

Migra on

.

Acclima on

.

Adapta on

.Fucusserratus

Highest responsivenessin Brittany

Adaptive value remains unknown

Seaweed meadows:Loss in warm-

temperate regionsArctic invasion?

Ancient refugiaunder threat:

stress in BrittanyExtinction risk in Spain

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Introduction Distributional changes Acclimation Adaptation Conclusions

Remaining key questions

Adaptation or acclimation to Arctic dark periods?Adaptation or extinction in genetically diverse ancient glacialrefugia?Role of epigenetics and microbiome for rapid adaptation?

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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). “Futureclimate change is predicted to shift long-term persistence zonesin the cold-temperate kelp Laminaria hyperborea.” In: MarineEnvironmental Research 113, pp. 174–182.

Braune, W (2008). Meeresalgen: ein Farbbildf{ü}hrer zuverbreiteten benthischen Gr{ü}n-, Braun- und Rotalgen derWeltmeere. Gantner.

Brodie, J, CJ Williamson, Da Smale, Na Kamenos,N Mieszkowska, R Santos, et al. (2014). “The future of thenortheast Atlantic benthic flora in a high CO2 world.” In:Ecology and Evolution 4.13, pp. 2787–2798.

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References

References II

Cock, JM, L Sterck, P Rouze, D Scornet, AE Allen, G Amoutzias,et al. (2010). “The \textit{{E}ctocarpus} genome and theindependent evolution of multicellularity in brown algae.” In:Nature 465.7298, pp. 617–621.

Dittami, SM, L Duboscq-Bidot, M Perennou, A Gobet, E Corre,C Boyen, et al. (2015). “Host-microbe interactions as a driver ofacclimation to salinity gradients in brown algal cultures.” In:The ISME journal 10.1, pp. 51–63.

Egan, S, T Harder, C Burke, P Steinberg, S Kjelleberg, T Thomas,et al. (2013). “The seaweed holobiont: understandingseaweed-bacteria interactions.” In: FEMS microbiology reviews37.3, pp. 462–76.

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References

References III

Hansen, MM, EE Nielsen, and KLD Mensberg (2006).“Underwater but not out of sight: genetic monitoring of effectivepopulation size in the endangered North Sea houting(\textit{Coregonus oxyrhynchus}).” In: Canadian Journal ofFisheries and Aquatic Sciences 63.4, pp. 780–787.

Harley, CDG, KM Anderson, KW Demes, JP Jorve, RL Kordas,TA Coyle, et al. (2012). “Effects of climate change on globalseaweed communities.” In: Journal of Phycology 48.5,pp. 1064–1078.

Hoarau, G, JA Coyer, M Giesbers, A Jueterbock, and JL Olsen(2015). “Pre-zygotic isolation in the macroalgal genus Fucusfrom four contact zones spanning 100–10 000 years: a tale ofreinforcement?” In: Royal Society Open Science 2.2, p. 140538.

@AJueterbock North Atlantic fucoids in the light of global warming 3 / 11

References

References IV

Hoarau, G, J Coyer, WT Stam, and JL Olsen (2007). “A fast andinexpensive DNA extraction/purification protocol for brownmacroalgae.” In: Molecular Ecology Notes 7, pp. 191–193.

Al-Janabi, B, I Kruse, A Graiff, U Karsten, and M Wahl (2016).“Genotypic variation influences tolerance to warming andacidification of early life-stage Fucus vesiculosus L.(Phaeophyceae) in a seasonally fluctuating environment.” In:Marine Biology 163.1, p. 14.

Jueterbock, A (2013). “Climate change impact on the seaweed\textit{Fucus serratus}, a key foundational species on NorthAtlantic rocky shores.” PhD thesis. 8049 Bod{ø}: University ofNordland.

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References

References V

Jueterbock, A, S Kollias, I Smolina, JMO Fernandes, JA Coyer,JL Olsen, et al. (2014). “Thermal stress resistance of the brownalga \textit{Fucus serratus} along the North-Atlantic coast:Acclimatization potential to climate change.” In: MarineGenomics 13, pp. 27–36.

Jueterbock, A, L Tyberghein, H Verbruggen, JA Coyer, JL Olsen,and G Hoarau (2013). “Climate change impact on seaweedmeadow 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). “Thefate of the Arctic seaweed Fucus distichus under climate change:an ecological niche modeling approach.” In: Ecology andEvolution, n/a–n/a.

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References

References VI

Krause-Jensen, D and CM Duarte (2016). “Substantial role ofmacroalgae in marine carbon sequestration.” In: NatureGeoscience 9.10, pp. 737–742.

Latzel, V, E Allan, A Bortolini Silveira, V Colot, M Fischer, andO Bossdorf (2013). “Epigenetic diversity increases theproductivity and stability of plant populations.” In: Naturecommunications 4, p. 2875.

Lourenço, CR, GI Zardi, CD McQuaid, Ea Serrão, Ga Pearson,R Jacinto, et al. (2016). “Upwelling areas as climate changerefugia for the distribution and genetic diversity of a marinemacroalga.” In: Journal of Biogeography, n/a–n/a.

McMahon, CR and GC Hays (2006). “Thermal niche, large-scalemovements and implications of climate change for a criticallyendangered marine vertebrate.” In: Global Change Biology 12.7,pp. 1330–1338.

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References

References VII

Müller, R, T Laepple, I Bartsch, C Wiencke, et al. (2009). “Impactof oceanic warming on the distribution of seaweeds in polar andcold-temperate waters.” In: Botanica Marina 52.6, pp. 617–638.

Nicastro, KR, GI Zardi, S Teixeira, JJ Neiva, EA Serrao,GA Pearson, et al. (2013). “Shift happens: trailing edgecontraction associated with recent warming trends threatens adistinct genetic lineage in the marine macroalga \textit{Fucusvesiculosus}.” In: BMC Biology 11.1, p. 6.

Pearson, Ga, A Lago-Leston, and C Mota (2009). “Frayed at theedges: Selective pressure and adaptive response to abioticstressors are mismatched in low diversity edge populations.” In:Journal of Ecology 97.3, pp. 450–462.

Phillips, SJ, RP Anderson, and RE Schapire (2006). “Maximumentropy modelling of species geographic distributions.” In:Ecological Modelling 190.3-4, pp. 231–259.

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References VIII

Provan, J and CA Maggs (2012). “Unique genetic variation at aspecies’ rear edge is under threat from global climate change.”In: Proceedings of the Royal Society of London Series B279.1726, pp. 39–47.

Raybaud, V, G Beaugrand, E Goberville, G Delebecq, C Destombe,M Valero, et al. (2013). “Decline in Kelp in West Europe andClimate.” In: PLOS ONE 8.6, e66044.

Saada, G, KR Nicastro, R Jacinto, CD McQuaid, EA Serrão,GA Pearson, et al. (2016). “Taking the heat: distinctvulnerability to thermal stress of central and threatenedperipheral lineages of a marine macroalga.” In: Diversity andDistributions 22.10. Ed. by D Schoeman, pp. 1060–1068.

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References IX

Smolina, I, S Kollias, A Jueterbock, JA Coyer, and G Hoarau(2016). “Variation in thermal stress response in two populationsof the brown seaweed, Fucus distichus, from the Arctic andsubarctic intertidal.” en. In: Royal Society Open Science 3.1,p. 150429.

Tyberghein, L, H Verbruggen, K Pauly, C Troupin, F Mineur, andO De Clerck (2012). “Bio-ORACLE: a global environmentaldataset for marine species distribution modelling.” In: GlobalEcology and Biogeography 21.2, pp. 272–281.

Ugarte, RA, A Critchley, AR Serdynska, and JP Deveau (2009).“Changes in composition of rockweed (\textit{Ascophyllumnodosum}) beds due to possible recent increase in seatemperature in Eastern Canada.” In: Journal of AppliedPhycology 21.5, pp. 591–598.

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References X

Viejo, RM, B Mart\’inez, J Arrontes, C Astudillo, andL Hernández (2011). “Reproductive patterns in central andmarginal populations of a large brown seaweed: drastic changesat the southern range limit.” In: Ecography 34.1, pp. 75–84.

Vitti, JJ, MK Cho, SA Tishkoff, and PC Sabeti (2012). “Humanevolutionary genomics: ethical and interpretive issues.” In:Trends in Genetics 28.3, pp. 137–145.

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References

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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