Range shifts and adaptive responses during ice ages and recent global warming with emphasis on the...

Ice ages Recent global warming Ice age responses The effect of the past Climate change responses Summary

Range shifts and adaptive responsesduring ice ages and recent global warming

with emphasis on thespecificity of the marine environment

Alexander Jü[email protected]

Faculty of Biosciences and AquacultureUniversity of Nordland

Trial lecture, 12.08.2013

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The origin of fjords -a hint to climate changes in the past

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Ice ages in earth history

Ice age periods

2.5 Mya

4.6 Bya3 / 52


Climate fluctuations causing species range shiftsMilankovich cycles

IPCC2007

Ocean currentsNOAA

CO2 fluctuations

Ice coverNASA

Climate fluctuationsNASA

Species distribution[Garrison T., 2010; Oceanography]

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The last ice age period started 2.5 Mya

[Andersen et al., 1997]

2.5 Mya

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Pleistocene ice agesN-Europe N-America

Weichsel Wisconsin

Eem Sangamon

Saale Illinoian

Holstein Yarmouth

Elster Kansan

Sea level changesOcean current changesMarine lakes and closed ocean gateways

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Atmospheric CO2 fluctuations played a major role

[Andersen et al., 1997]7 / 52


Ocean acidification - the other CO2 problem

[Pelejero et al., 2010; Trends Ecol. Evol.]

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Recent land and ocean warming

Christiansen, J.; Scientific American (2013)

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Recent climate change vs. Pleistocene ice ages

Higher CO2concentration(Anthropogenic)

Ahlenius, H.; UNEP/GRID-Arendal10 / 52


Predicted temperature increase

[Meehl et al., 2007; IPCC]

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3℃ in next 200 yrs





3℃ in next 200 yrs 2–4 times faster



The present is the key to the past— James Hutton and Charles Lyell

The pastis the key to the presentis the key to the future

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Responses in the past

[Davis & Shaw, 2001; Science]

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Responses in the pastLong-distance dispersers Poor dispersers

[Garrison T., 2010; Oceanography][Garrison T., 2010; Oceanography]

Fucus serratus

Littorina saxatilis[Johannesson et al., 1993; Evolution ]

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80% of marine species with planktonic life stages

[Tardent (2005)]16 / 52


Pelagic life stages allow for high gene flowBE

NTHO

SPL

ANKT

ON

Population 1 Population 3Population 2

adults adults adults

larvae

Population admixture

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Habitat trackingthrough high population connectivity

Palaeo-distribution ofCalanus finmarchicus

[Provan et al., 2009; Proc. R. Soc. London, Ser. B]

SST during the LGM[Meland et al., 2005; Quat. Sci. Rev.]

[Hansen et al., 2008; Gen. Comp. Endocr.]

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Habitat trackingthrough high population connectivity

359,000–566,000 YBP

Absolute Ne > 100, 000,suggesting high adaptive capacity

[Provan et al., 2009; Proc. R. Soc. London, Ser. B]

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Potential gene flow barriers for planktonic speciesBE

NTHO

SPL

ANKT

ON

Population 1 Population 3Population 2

adults adults adults

larvae larvae larvae

Population admixture Larval recruitmentPhysical barriers

Intrinsic barriers

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Gene flow limits during glacial periodsPotential allopatric differentiation in a holoplankonic diatom

Dispersal barrier

Geographic distribution of Pseudo-nitzschia pungens- relies on coastal regions

[Casteleyn, 2010; Proc. R. Soc. London, Ser. B]

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Gene flow limits during glacial periodsPotential allopatric differentiation in a holoplankonic diatom

Divergence time estimates (My) among Pseudo-nitzschia speciesbased on ITS, rbcL and LSU rDNA

[Casteleyn, 2010; Proc. R. Soc. London, Ser. B]20 / 52



Long-distance dispersers Poor dispersersN

Habitat trackingPopulation subdivision

[Garrison T., 2010; Oceanography]

Fucus serratus

Littorina saxatilis[Johannesson et al., 1993; Evolution ]

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Retraction into glacial refugia in the North Atlantic

Refugia in Ireland and the “Hurd Deep”

[Maggs et al., 2008; Ecology]

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southern richness

northern purity

Refugia in Ireland and the “Hurd Deep”

[Maggs et al., 2008; Ecology]22 / 52



Refugia in Ireland and the “Hurd Deep”[Maggs et al., 2008; Ecology]

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Identification of refugia

unique allelesin mid-range

Refugia in Ireland and the “Hurd Deep”[Maggs et al., 2008; Ecology]

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Adaptation to empty niches during recolonization

Rapid speciation in the postglacial Baltic Sea[Pereyra et al., 2009; BMC Evol. Biol.]

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Adaptation to empty niches during recolonization

Neighbour-joining tree based on 9 microsatellites

F. radicans emerged as a monophyletic taxon ca. 400 yrs ago[Pereyra et al., 2009; BMC Evol. Biol.]

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Habitat trackingExtinction, recolonization

Niche adaptationSpeciation

Refugia

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The effect of the past responses on presentcharacteristics

N

Long-distance dispersersPoor dispersers

Population age, Ne,genetic diversity, adaptability Evolvability

or or

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Effective population size and adaptability

Pearson, 2008 [Frankham et al., 2002; Conserv. Gen.]

Low Ne : Loss of genetic diversity due to genetic drift

Ne >500 to maintain sufficient evolutionary potentialRate of evolution and population persistence depend on Ne

[Moya et al., 2000; PNAS] [Frankham et al., 2002; Conserv. Gen.] 28 / 52


High adaptive potential in long-distance dispersers

[Peijnenburg & Goetze, 2013; Ecol. Evol.]

Ne up to 107–1015 High effectiveness ofselection over genetic drift

Short generation time Rapidevolutionary response

(e.g. 500 generations for increased fitnessunder ocean acidification in the coccolithophoreEmiliania huxleyi)[Lohbeck et al., 2012; Nature Geoscience]

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N



or or

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Genetic diversity can increaseclimate change resilience

[Ehlers et al., 2008; Mar. Ecol. Prog. Ser.]

no growthlethal

[Reusch et al., 2005; Proc. Natl. Acad. Sci. U.S.A.]

Genetic diversity increased recovery of seagrass (Zostera marina)beds after the 2003 European heat wave (Baltic sea)

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N



or or

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Saltatory evolutionary changes at the leading edge

Open habitat New mutationRecolonization

Allele 1Allele 2

Surfing of new allelic variations (neutral, deleterious or advantageous)at the expanding range edge

[Excoffier et al., 2009; Annu. Rev. Ecol. Evol. Syst.]33 / 52


Extensive introgression during range expansion

Network and distribution of mtIGS (organelle sequence)in F. ceranoides

[Neiva et al., 2010; Mol. Ecol.]

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Climate change responsesLong-distance dispersers Poor dispersers

N

Habitat tracking?

Yes: 19 km yr−1

Adaptation?

Phenology in Arctic

Refugia stable?

No

Northward shift?

Assemblage shifts,evolution?

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Marine (oceanic) range shiftscan track isotherm shifts

Average shift: 23 km yr−1

[Beaugrand et al., 2009; Glob. Change Biol.]

Isotherm shift

15℃ isotherm shift at 22 km yr−1

(330 km from 1983 to 2003)[McMahon & Hays, 2006; Glob. Change Biol.]

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Range shift pronounced in marine species

Species range shift

Terrestrial 0.61 km yr−1 ± 0.24 SE99 species of birds, butterflies and alpine herbs[Parmesan & Yohe, 2003; Nature]

Marine 19 km yr−1 ± 3.8 SE73 species of phytoplankton, seaweeds, sponges, corals, bivalves,gastropods, barnacles, crabs, fishes etc. [Sorte et al., 2010; Oikos]

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N

Habitat tracking?Yes: 19 km yr−1

Adaptation?

Phenology in Arctic

Refugia stable?

No

Northward shift?


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Selection pressure highest in the Arctic

Strongest temperature increase and limited retreatLow thermal variability - favoring cold-thermal specialistsBig seasonality shifts

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Mean sea surface temperature anomaly(2001–2005 relative to 1951–1980)

[Hansen et al., 2006; Can. J. Fish. Aquat. Sci.]

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Strongest temperature increase and limited retreatLow thermal variability - favoring cold-thermalspecialistsBig seasonality shifts

[Dam, 2013; Annu. Rev. Mar. Sci.]39 / 52




Seasonality shifts (days/decade) in the change of timing for Apriltemperatures (N: spring, S: fall)

[Burrows, 2011; Science]

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Genetically based phenology shiftsAdaptive responses to climate change in terrestrial species

Yukon red squirrel(Tamiascurus hudsonicus):

Advancement ofreproduction time

Pitcher-plant mosquito(Wyeomyia smithii):

Shift of larval dormancyto shorter day lengths

[Bradshaw & Holzapfel, 2006; Science]

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Phenology shifts pronounced in marine taxa

Terrestrial taxa:5.1 days decade−1

[Root et al., 2003; Nature]

Zooplankton:7 days decade−1

[Richardson et al., 2008; Science]

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Phenology shifts in marine taxa

Potential mismatch in timing between trophic levels

Changes in timing of seasonal peaks (in months)in 66 taxa in the North Sea[Edwards & Richardson, 2004; Nature]

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Trophical mismatch in the Arctic

Calanus glacialis

Offspring exploit phytoplankton bloom[Søreide et al., 2010; Global Chang. Biol.]

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Trophical mismatch in the Arctic

Calanus glacialis

Earlier onset of spring bloom:Selection pressure on the rate of development

[Søreide et al., 2010; Global Chang. Biol.]

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N


Adaptation?Phenology in Arctic

Refugia stable?

No

Northward shift?


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Threatened refugial populations

Based on mitochondrial SNPs

[Provan & Maggs, 2012; Proc. R. Soc. London, Ser. B]

Chondrus crispus: 180 kmretreat since 1971 froma Portuguese refugium

Interglacial distribution

Glacial distribution

Stable refugiumunder threat

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Threatened refugial populations

[Jueterbock et al., 2013; Ecol. Evol.]

[Hoarau et al., 2007; Mol. Ecol.]

[Viejo et al., 2011; Ecography]Dwarf forms withreduced reproduc-tive capacity inSpain

Fucus serratus

Predicted extinctionfrom ancient refugia by2200

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N



Refugia stable?No

Northward shift?


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Predicted invasion intensity until 2050Opening up of new habitat in the Arctic

Predicted invasion intensity(1066 species of fish and invertebrates)

in 2050 relative to the mean of 2001–2005[Cheung et al., 2009; Fish and Fisheries]

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Climate change responses




Refugia stable?No

Northward shift?Dispersal, colonization?

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Global warming has a stronger impact thanpleistocene warm periods



Ahlenius, H.; UNEP/GRID-Arendal

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Global warming has a stronger impact thanpleistocene warm periods



Additional stressors

Ahlenius, H.; UNEP/GRID-Arendal

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Human impact on marine ecosystems

Cumulative human impact[Halpern et al., 2010; Science]

ShippingEutrophicationPollutionUV radiationOverfishing

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SummaryRange shifts and evolutionary (adaptive) shifts are connected

Long-range dispersers Poor dispersers

Past response Habitat tracking Extinction, recolonizationPopulation subdivision Niche adaptation, speciation

Ne, genetic diversity Higher Lower, centeredAdaptation potential High Centered in refugiaClimate change Habitat tracking Loss of refugia

Arctic adaptation? Stochastic evolution

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Ne, genetic diversity Higher Lower, centered

Adaptation potential High Centered in refugiaClimate change Habitat tracking Loss of refugia


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Ne, genetic diversity Higher Lower, centeredAdaptation potential High Centered in refugia

Climate change Habitat tracking Loss of refugiaArctic adaptation? Stochastic evolution

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Ne, genetic diversity Higher Lower, centeredAdaptation potential High Centered in refugiaClimate change Habitat tracking Loss of refugia


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References Appendix

References I

Andersen, B.G; Borns, H.W. (1997)The Ice Age world: an introduction to Quaternary history and research with emphasis on North Americaand northern Europe during the last 2.5 million yearsScandinavian University Press

Beaugrand, G.; Luczak, C. & Edwards, M. (2009): Rapid biogeographical plankton shifts in the NorthAtlantic Ocean.Glob. Change Biol. 15(7):1790–1803.

Bradshaw, W. E. & Holzapfel, C. M. (2006): Climate change - evolutionary response to rapid climatechange.Science 312(5779):1477–1478.

Bradshaw, W. E. & Holzapfel, C. M. (2008): Genetic response to rapid climate change: it’s seasonal timingthat matters.Mol. Ecol. 17(1):157–66.

Burrows, M. T.; Schoeman, D. S.; Buckley, L. B; Moore, P.; Poloczanska, E. S.; Brander, K. M.; Brown,C.; Bruno, J. F.; Duarte, C. M.; Halpern, B. S. (2011)The pace of shifting climate in marine and terrestrial ecosystemsScience 334(6056):652–655.

Casteleyn, G.; Leliaert, F.; Backeljau, T.; Debeer, A.-E.; Kotaki, Y.; Rhodes, L.;(2010): Limits to gene flowin a cosmopolitan marine planktonic diatom.Proc. R. Soc. London, Ser. B 107(29):12952–12957.

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References Appendix

References II

Cheung, W. W. L.; Lam, V. W. Y.; Sarmiento, J. L.; Kearney, K.; Watson, R.; Pauly, D. (2009): Projectingglobal marine biodiversity impacts under climate change scenariosFish and Fisheries 10(3):235–251.

Dam, H.G. (2013)Evolutionary Adaptation of Marine Zooplankton to Global ChangeAnnual Review of Marine Science 5(1):349–370.

Davis, M.B.; Shaw, R.G. (2001)Range shifts and adaptive responses to quaternary climate changeScience 292(5517):673–679.

Edwards, M. & Richardson, A. (2004): Impact of climate change on marine pelagic phenology and trophicmismatch.NATURE 430(7002):881–884.

Ehlers, A.; Worm, B. & Reusch, T. B. H. (2008): Importance of genetic diversity in eelgrass Zostera marinafor its resilience to global warming.Mar. Ecol. Prog. Ser. 355:1–7.

Excoffier, L.; Foll, M.; Petit, R.J. (2009): Genetic Consequences of Range ExpansionsAnnu. Rev. Ecol. Evol. Syst. 40(1).

Frankham, R; Ballou, J.D.; Briscoe, D.A. (2002)Introduction to Conservation Genetics Cambridge University Press

Garrison, T. (2010)Oceanography

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References Appendix

References III

Halpern, B.S.; Walbridge, S.; Selkoe, K.A.; Kappel, C.V.; Micheli, F.; D’Agrosa, C.; Bruno, J.F.; Casey,K.S.; Ebert, C.; Fox, H.E. and others (2010)A global map of human impact on marine ecosystemsScience 319(5856):948–952.

Hampe, A. & Petit, R. J. (2005): Conserving biodiversity under climate change: the rear edge matters.Ecol. Lett. 8(5):461–467.

Hansen, M. M.; Nielsen, E. E. & Mensberg, K.-L. D. (2006): Underwater but not out of sight: geneticmonitoring of effective population size in the endangered North Sea houting (Coregonus oxyrhynchus).Can. J. Fish. Aquat. Sci. 63(4):780–787.

Hansen, B.H.; Altin, D.; Hessen, K.M.; Dahl, U.; Breitholtz, M.; Nordtug, T. (2008)Expression of ecdysteroids and cytochrome P450 enzymes during lipid turnover and reproduction in Calanusfinmarchicus (Crustacea: Copepoda)General and Comparative Endocrinology 158(1):115–121.

Hoarau, G.; Coyer, J.A.; Veldsink, J.H.; Stam, W.T.; Olsen, J.L. (2007)Glacial refugia and recolonization pathways in the brown seaweed Fucus serratusMolecular Ecology 16(17):3606–3616.

Hughes, Terry P; Baird,;Andrew H; Bellwood, David R; Card, Margaret; Connolly, Sean R; Folke, Carl;Grosberg, Richard; Hoegh-Guldberg, Ove; Jackson, JBC; Kleypas, Janice; others (2003)Climate change, human impacts, and the resilience of coral reefsScience 301(5635):929–933.

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References Appendix

References IV

Solomon, S.; Qin, D.; Manning, M.; Chen, Z.; Marquis, M.; Averyt; K.B.; Tignor, M.; Miller, H.L. (eds)(2007)Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the FourthAssessment Report of the Intergovernmental Panel on Climate ChangeCambridge University Press, Cambridge, United Kingdom and New York, NY, USA

Johannesson, K.; Johannesson, B.; Rolan-Alvarez, E. (1993)Morphological differentiation and genetic cohesiveness over a microenvironmental gradient in the marinesnail Littorina saxatilisEvolution 47(6):1770–1787.

Jueterbock, A.; Tyberghein, L.; Verbruggen, H.; Coyer, J. A.; Olsen, J. L. & Hoarau, G. (2013): Climatechange impact on seaweed meadow distribution in the North Atlantic rocky intertidal.Ecol. Evol. 3(5):1356–1373.

Laing, A.; Evans, J.L. (2010)Introduction to tropical meteorologyThe COMET Program

Lohbeck, K.T.; Riebesell, U.; Reusch, T.B.H. (2012): Adaptive evolution of a key phytoplankton species toocean acidificationNature Geoscience 5(5):346–351.

Maggs, C. A.; Castilho, R.; Foltz, D.; Henzler, C.; Jolly, M. T.; Kelly, J.; Olsen, J.; Perez, K. E.; Stam, W.;Väinölä, R. et al. (2008): Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa.Ecology 89:108–122.

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References Appendix

References V

McMahon, C. R. & Hays, G. C. (2006): Thermal niche, large-scale movements and implications of climatechange for a critically endangered marine vertebrate.Glob. Change Biol. 12(7):1330–1338.

Meehl, G. A.; Stocker, T. F.; Collins, W. D.; Friedlingstein, P.; Gaye, A. T.; Gregory, J. M.; Kitoh, A.;Knutti, R.; Murphy, J. M.; Noda, A.; Raper, S. C. B.; Watterson, I. G.; Weaver, A. J. & Zhao, Z.-C.(2007): Global Climate Projections.S. Solomon; D. Qin; M. Manning; Z. Chen; M. Marquis; K. B. Averyt; M. Tignor & H. L. Miller (editors),Climate Change 2007: the physical science basis: contribution of working group I to the fourth assessmentreport of the intergovernmental panel on climate change, pages 749–846. Cambridge University Press,Cambridge, United Kingdom and New York, NY, USA.

Meland, M.Y.; Jansen, E.; Elderfield, H. (2005): Constraints on SST estimates for the northern NorthAtlantic/Nordic Seas during the LGMQuarternary Science Reviews 24(7–9):835–852.

Moya, A.; Elena, Elena, S.F.; Bracho, A.; Miralles, R.; Barrio; E. (2000)The evolution of RNA viruses: a population genetics viewProceedings of the National Academy of Sciences 97(13):6967–6973.

Neiva, J; Pearson, G.,A.; Valero, M.; Serrão, E. A. (2010): Surfing the wave on a borrowed board: rangeexpansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L.Molecular Ecology 19(21):4812–4822.

Parmesan, C. and Yohe, G. (2003)A globally coherent fingerprint of climate change impacts across natural systemsNature 421(6918):37–42.

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References Appendix

References VI

Peijnenburg, K. T. C. A. and Goetze, E. (2013): High evolutionary potential of marine zooplanktonEcology and Evolution

Pelejero C.; Calvo, E.; Hoegh-Guldberg, O. (2010)Paleo-perspectives on ocean acidificationTrends in Ecology & Evolution 25(6):332–344.

Pereyra, R. T.; Bergström, L.; Kautsky, L. & Johannesson, K. (????): Rapid speciation in a newly openedpostglacial marine environment, the Baltic Sea.BMC Evol. Biol. 9(1):70.

Perry, A. L.; Low, P. J.; Ellis, J. R.; Reynolds, J.D. (2005)Climate change and distribution shifts in marine fishesScience 308(5730):1912–1915.

Provan, J. & Maggs, C. A. (2012): Unique genetic variation at a species’ rear edge is under threat fromglobal climate change.Proc. R. Soc. London, Ser. B 279(1726):39–47.

Provan, J.; Beatty, G. E.; Keating, S. L.; Maggs, C. A.; Savidge, G. (2009): High dispersal potential hasmaintained long-term population stability in the North Atlantic copepod Calanus finmarchicusProc. R. Soc. London, Ser. B 276(1655):301–307.

Reusch, T.; Ehlers, A.; Hammerli, A. & Worm, B. (2005): Ecosystem recovery after climatic extremesenhanced by genotypic diversity.Proc. Natl. Acad. Sci. U.S.A. 102(8):2826–2831.

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References Appendix

References VII

Richardson, A. J.; Poloczanska, E. S. et al. (????): Under-resourced, under threat.SCIENCE 320(5881):1294.

Root, T. L.; Price, J. T.; Hall, K. R.; Schneider, S. H.; Rosenzweig, C. & Pounds, J. A. (2003): Fingerprintsof global warming on wild animals and plants.Nature 421(6918):57–60.

Søreide, J. E.; Leu, E.; Berge, J.; Graeve, M.; Falk-Petersen, S. (2010): Timing of blooms, algal foodquality and Calanus glacialis reproduction and growth in a changing ArcticGlobal Chang. Biol. 16(11):3154–3163.

Sorte, C. J. B.; Fuller, A. & Bracken, M. E. S. (2010): Impacts of a simulated heat wave on composition ofa marine community.Oikos 119(12):1909–1918.

Sunday, J. M.; Crim, R.; Harley, C. D. G.; Hart, M. W. (2011): Quantifying Rates of EvolutionaryAdaptation in Response to Ocean AcidificationPLoS ONE 6(8):e22881.

Sunday, J. M.; Bates, A. E. & Dulvy, N. K. (2012): Thermal tolerance and the global redistribution ofanimals.Nat. Clim. Chang. 2(9):686–690.

Tardent, P. (2005): Meeresbiologie : eine Einführung.Thieme, Stuttgart [u. a.]

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References Appendix

References VIII

Tomanek, L. (2010): Variation in the heat shock response and its implication for predicting the effect ofglobal climate change on species’ biogeographical distribution ranges and metabolic costs.J. Exp. Biol. 213(6):971–979.

Viejo, R. M.; Martínez, B.; Arrontes, J.; Astudillo, C. & Hernández, L. (2011): Reproductive patterns incentral and marginal populations of a large brown seaweed: drastic changes at the southern range limit.Ecography 34(1):75–84.

Wernberg, T.; Russell, B. D.; Moore, P. J.; Ling, S. D.; Smale, D. A.; Campbell, A.; Coleman, M. A.;Steinberg, P. D.; Kendrick, G. A. & Connell, S. D. (2011): Impacts of climate change in a global hotspotfor temperate marine biodiversity and ocean warming.J. Exp. Mar. Biol. Ecol. 400(1–2):7–16.

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References Appendix

Admixture of ancient refugiaincreases diversity in the north


Based on cytochrome b data

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References Appendix

Identification of refugia

Evidence for a Canadian refugium


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References Appendix

Evolutionary rates of zooplankton largely unknown

Response to selection (acidification from pH 8.3 to 7.9): R = h2 ∗ S

Strongylocentrotus franciscanusMytilus trossolus

Genetic and phenotypic diversity increasesthe selection differential S, (h2:0–0.14)

[Sunday et al., 2011; PLoS ONE]

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References Appendix

Thermal caused range shifts in marine fishes

Species with faster life histories shifted more rapidly northwards or to greater depthsin the North Sea

(2–16 km yr−1, 15 shifting species, 21 non-shifting species, 6℃ warming between1962 and 2001)

[Perry et al., 2005; Science]

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References Appendix

Sensitivity of the southern range limit of marineectotherms

Realized and potential latitudinal distributions[Sunday et al., 2012; Nat. Clim. Chang.]

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References Appendix

Range-edge characteristics

[Hampe & Petit, 2005; Ecol. Lett.]

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References Appendix

Marine range shifts (190 km decade−1)can track isotherm shifts

Average poleward migration rate ofisotherms: 38 km decade−1

[Hansen et al., 2006; Can. J. Fish. Aquat. Sci.]

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References Appendix

What explains the strong range shift of marine taxa?

Marine TerrestrialThermal variability Low HighSouthern thermal range Filling UnderfillingSeasonality and isotherm shifts Faster SlowerRange limits Few More

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References Appendix

What explains the strong range shift of marine taxa?Marine Terrestrial

Thermal variability Low HighSouthern thermal range Filling UnderfillingSeasonality and isotherm shifts Faster SlowerRange limits Few More

[Laing & Evans, 2010] 16 / 19

References Appendix

What explains the strong range shift of marine taxa?Marine Terrestrial

Thermal variability Low HighSouthern thermal range Filling UnderfillingSeasonality and isotherm shifts Faster SlowerRange limits Few More

[Sunday et al., 2012; Nat. Clim. Chang.]

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References Appendix

What explains the strong range shift of marine taxa?

Marine TerrestrialThermal variability Low HighSouthern thermal range Filling UnderfillingSeasonality and isotherm shifts Faster SlowerRange limits Few More

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References Appendix

Poleward retreat and extinction of seaweeds inSouth-Australia

[Wernberg et al., 2011; J. Exp. Mar. Biol. Ecol.]

Shift of up to 2° latitudePredicted extinction of 25% seaweed species

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References Appendix

Coral bleaching

Additional stress:Degraded water qualityOverharvesting of herbivorousgrazers

[Hughes et al., 2003; Science]

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References Appendix

Potential causes of climate fluctuationsMilankovich cycles as trigger

[Andersen et al., 1997] 19 / 19

Range shifts and adaptive responses during ice ages and recent global warming with emphasis on the...

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