DOI: 10.1126/science.1225345, 742 (2012);338 Science

et al.Hilary H. BirksScandinavia''Comment on ''Glacial Survival of Boreal Trees in Northern

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Comment on “Glacial Survivalof Boreal Trees inNorthern Scandinavia”Hilary H. Birks,1* Thomas Giesecke,2 Godfrey M. Hewitt,3 Polychronis C. Tzedakis,4

Jostein Bakke,5 H. John B. Birks1,4,6

Parducci et al. (Reports, 2 March 2012, p. 1083) fail to present convincing evidence for glacialsurvival of Pinus and Picea in northern Scandinavia. Their methodology does not excludecontamination. Additionally, they should consider the lack of suitable habitats, the apparentextinction of both taxa after deglacial warming, and alternative hypotheses for the distribution ofthe Picea genetic marker haplotype A.

Parducci et al. (1) propose thatPicea (spruce)and Pinus (pine) survived the Last GlacialMaximum (LGM) in northern Scandinavia,

based on the amplification of ancient chloroplastDNA (cpDNA) in lake sediments fromEndletvatnon the Andøya strandflat, northwest Norway(69°N) and genetic evidence from extant sprucepopulations. We comment first on their method-ology and then on their interpretations.

(i) How reliable is ancient DNA (aDNA) fromlake sediments? Although knowledge of aDNA, in-cluding sedimentary aDNA (sedaDNA), and envi-ronmental DNA is advancing rapidly, Hofreiter et al.(2) warn that the reliability of all aDNA sequencesmust be critically assessed, major concerns beingcontamination and the variable quality of aDNAfrom waterlogged sites. They urge “a critical atti-tude towardswhether the results obtained domakesense.” This new technique was apparently not vali-dated byParducci et al., who ignored the criteria andadvice of Gilbert et al. (3) to minimize contami-nation and replicate results.

The Geonor stationary-piston sediment corer,like most piston corers, is not a contamination-free corer. A contamination-free corer (4) shouldhave been used.

The core studied by Parducci et al. was openedin 2002, sampled, and stored at 4°C for 7 yearsuntil sampled for DNA. How certain is it that nocontamination occurred during potentiallyunsterile sampling in 2002 from aerial pollen,dust, wood, or paper? The reported contamina-tion by an Urtica plant fragment is worrying.

(ii) Was glacial survival on Andøya possible?The LGM ice sheet advanced over Andøya, in-cluding Endletvatn, reaching a 2- to 300-m altitude.Mountain glaciers left only the highest summitsand plateaus as ice-free nunataks (5). These aremostly covered by block fields (5), which are notsuitable habitats today for Picea or Pinus. As iceretreated at ~22 thousand years ago (ka), the ex-tensive lowlands, including Endletvatn, were be-low sea level until a marine regression ~18 ka (5).Glacial and marine conditions prevailed atEndletvatn at the times of the cpDNA records.

(iii) Where were Pinus and Picea growing?They could not survive on exposed nunataks in theinferred polar-desert conditions (1, 6). Picea, butnot Pinus,may persist vegetatively for centuries insheltered locations. To deliver DNA to the lake,they should have grown nearby, but the strandflatwas glaciated or submerged (driftwood could pro-vide aDNA) at the critical periods. Therefore, wheredid the cpDNA come from? Willerslev et al. (7)proposed long-distance dispersal of conifer DNAto Greenland ice. Likewise, extremely low Pinusvalues in Andøya pollen diagrams could derivefrom long-distance dispersal. The rather surpris-ing absence of conifer pollen in their samples ledParducci et al. to exclude this source.

(iv) Does haplotype A (HapA) reflect Piceaspreading directions? Early Holocene Picea mi-tochondrial DNA (mtDNA) from lake sedimentand younger pollen in Trøndelag shows HapA(1), probably a single 21–base pair deletion.Western glacial survival is inferred from its moderndistribution. Old cpDNA fromAndøya can provideno support for this hypothesis. The distribution ofother mtDNA and nuclear DNA markers (8)—combined with palaeoecological evidence ofsmall scattered, perhaps palynologically silent,early Picea populations in Scandinavia (9), in-cluding a possible Late Glacial (but not LGM)occurrence on a Swedish nunatak (10)—suggestseveral immigrations along both northern andsouthern routes after deglaciation. This scenariowould explain the observed genetic diversitiesfromRussia to Scandinavia (8). Furthermore, LGM

Picea populations south of the icewithHapA couldhave spread north during deglaciation, meanwhilebecoming extinct in their southern refugia. Pop-ulations only expanded after ~3000 years beforethe present (BP) (9). HapA could have arisen in apioneer southern population, increased in smallpopulations, and spread toward the west and north,mixing with lineages sharing HapB. Multipleimmigrations from western and southern direc-tions would tend to block the spread of the north-ern ones (11). Even if HapA survived onAndøya,it would be unlikely to spread southward. Al-though Parducci et al. argue that a distinct geno-type cluster in central Scandinavian populations(8) indicates a western origin, they should alsoconsider the several different genotype clusters inScandinavia that may be explained by leading-edge and surfing phenomena. Interestingly, theseclusters map poorly with HapA, but the spatialresolution is coarse. To clarify colonization pro-cesses, more sampling and genetic analyses areneeded to map the distribution of other individualmutations and markers. Parducci et al. demon-strate that Picea’s history in Scandinavia wasprobably more complex than previously thought,but they cannot claim that the lineage of the wide-spread HapA survived in northern Scandinaviaand spread south and east.

(v)Why arePinus andPicea absent onAndøyaafter 17,700 years BP? Late-Pleniglacial refugialtree populations with low palynological presencetypically respond to deglacial warming with in-creases in pollen percentages. For example, lowPleniglacial Picea pollen percentages at LakeGalich, in northern Russia, increased to morethan 20% during the Late Glacial interstadial(12). No Late Glacial expansion of Picea andPinus is recorded on Andøya (6), and neithergrew on Andøya during the early Holocene (13).Picea’s present northwestern limit is ~500 km tothe south (14). Andøya’s cool oceanic climatetoday does not support Picea, and Pinus is rare(14). It must have been much more inhospitableduring the glacial period, with a climate resem-bling that of Svalbard today (6).

We conclude that Parducci et al. have notjustified in sufficient detail “how their data wereobtained and why they should be believed to beauthentic” (3). Their methodology is question-able, due to the unsuitable corer, the age andstorage conditions of the sediment core, and thepotentially unsterile sampling. The taphonomy ofDNA in lake sediment needs rigorous investiga-tion. One cpDNA record of Picea and two ofPinus are insufficient to postulate glacial surviv-al. No account was taken of the lack of suitablehabitats on Andøya during the glacial period.Other parts of northern Scandinavia were ice-covered. The absence of Pinus and Picea duringthe deglacial and Holocene is contrary to all eco-logical expectations if small LGM populationssurvived near Endletvatn. The distribution of PiceamtDNA haplotypes can bemore readily explainedby postglacial colonization than by a northern

TECHNICALCOMMENT

1Department of Biology, University of Bergen,NO-5020Norway.2Department of Palynology and Climate Dynamics, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen,37073 Göttingen, Germany. 3Biological Sciences, University ofEast Anglia, Norwich NR4 7TJ, UK. 4Environmental ChangeResearch Centre, Department of Geography, University CollegeLondon, Gower St. LondonWC1E 6BT, UK. 5Department of EarthSciences, University of Bergen, NO-5007 Norway. 6Depart-ment of Geography and the Environment, University of Oxford,OX1 3QY, UK.

*To whom correspondence should be addressed. E-mail:hilary.birks@bio.uib.no

9 NOVEMBER 2012 VOL 338 SCIENCE www.sciencemag.org742-a

LGM refuge.We consider the evidence presentedby Parducci et al. to be unconvincing, so we re-ject their hypothesis that Picea and Pinus survivedthe last glacial period in northern Scandinavia.

References1. L. Parducci et al., Science 335, 1083 (2012).2. M. Hofreiter, M. Collins, J. R. Stewart, Quat. Sci. Rev. 33,

1 (2012).

3. M. T. P. Gilbert, H.-J. Bandelt, M. Hofreiter, I. Barnes,Trends Ecol. Evol. 20, 541 (2005).

4. D. T. Feek, M. Horrocks, W. T. Baisden, J. Flenley,J. Paleolimnol. 45, 115 (2011).

5. T. O. Vorren, L. Plassen, Boreas 31, 97 (2002).6. T. Alm, Boreas 22, 171 (1993).7. E. Willerslev, A. J. Hansen, B. Christensen,

J. P. Steffensen, P. Arctander, Proc. Natl. Acad. Sci. U.S.A.96, 8017 (1999).

8. M. M. Tollefsrud et al., Heredity 102, 549 (2009).9. T. Giesecke, K. D. Bennett, J. Biogeogr. 31, 1523 (2004).

10. L. Kullman, J. Biogeogr. 29, 1117 (2002).11. J. M. Waters, Mol. Ecol. 20, 4388 (2011).12. A. A. Velichko et al., Ser. Geographiheskaya 3, 42 (2001)

(in Russian).13. K.-D. Vorren, E. Elverland, M. Blaauw, E. K. Ravna,

C. A. H. Jensen, Boreas 38, 401 (2009).14. A. Moen, National Atlas of Norway: Vegetation

(Norwegian Mapping Authority, Hønefoss, 1999).

29 May 2012; accepted 4 September 201210.1126/science.1225345

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TECHNICAL COMMENT