Fig. 6: DIYABC Scenario 9 - Events and marine isotope stage (MIS)
assignment
According to our results from the ABC, the calibrated times of
demographic events can be assigned to marine isotope stages (MIS;
Railsback 2006) (Fig. 6). The first larch colonization (t4, population
N1a) has been recorded at around 224,000 years BP, which is equivalent
to MIS7 and specified as a moderate interglacial. This suggests that the
climate was favorable for larch establishment. The subsequent ancient
and severe bottleneck (t4-db, population N1a to population N1) can be
dated to 161,750 years BP, corresponding to MIS6, when the penultimate
glacial period occurred, which was a more severe glaciation than the
LGM. These harsh climate conditions may have caused loss of diversity
and a decrease in population size. The population N1a may have been
threatened with extinction, but after the bottleneck event, the
population size increased again. The subsequent split event (t3) is
registered at 32,000 years BP within MIS2, containing the LGM. This
period of moderate glaciation did not cause a significant decrease in
population size. The following split event (t2) and the admixture event
(t1) can be dated at 11,700 years BP and 4,175 years BP, respectively,
both in MIS1, thus in the Holocene. The split events and the higher
population size indicate better conditions such as greater fitness of
pollen or faster growth.
The ABC leads to the assumption that the common ancestors of today’s
larch populations (N1 and N2) must have been present in northeast
Siberia long before the last glacial. However, the exact timing of both
recent and ancient historical events should be considered a rough
estimate because of possible biases, as it is difficult to estimate the
average generation time of long-lived trees. Because the generation time
is likely to be greater than 25 years during colder climate stages, the
inferred divergence time is most probably underestimated. Hence, we can
deduce that larch populations must have survived in isolated refugia
during the last glacial. This hypothesis is also supported by similar
findings in other genetic studies that suggest the presence of several
refugia during Pleistocene glacial intervals (Polezhaeva et al. 2010;
Semerikov et al. 2013). Both pollen and macrofossil evidence indicates
the survival of Larix in northern regions throughout the LGM in
multiple and often isolated refugia (Khatab et al. 2008; Binney et al.
2009; Müller et al. 2010). Furthermore, we detected a genetic
differentiation that serves as an indicator of the mentioned long-term
isolation of the recent populations within geographically disconnected
refugia (Tóth et al. 2019). For Alaska, there are also indications of a
possible in situ persistence of larches during the LGM (Napier et al.
2020). Binney et al. (2017) mention that northern Eurasia is
topographically complex so it is likely that the wide range of local
climates provided conditions for refugial populations to persist. In the
region of the Eastern Yakutian cluster, the sheltered valleys of the
Verkhoyansk Mountains (Tarasov et al. 2009) or the Tschuch’ye Lake area
in Eastern Yakutia with its deep protected valleys (Lozhkin et al. 2018)
could have provided shelter for
the persistence of Larix during the LGM.
Our ABC shows that the populations that persisted during the LGM in
northern refugia have genetically contributed to post-LGM
recolonization. This is also corroborated by other studies that suggest
that these populations were established well before the LGM from a
single source population (Western Siberia) with probably a small
effective size and low recent gene flow (Ma et al. 2020; Semerikov et
al. 2013). The population in Chukotka probably originated earlier and
the population in Eastern Yakutia subsequently emerged in the course of
an admixture event of the populations from Western Yakutia and Chukotka.
However, our results contradict the conclusions of Schulte et al.
(2022b), who state that L. sibirica had to recolonize northern
areas from refugia in the south in the postglacial. It is possible thatL. sibirica retreated locally from the region of the lake
investigated in their study during the LGM but survived the LGM in other
northern areas. In general, the existing refugia are likely to have
strongly assisted the colonization of more northerly areas of the
forest-tundra ecotone since they provide a seed source and shelter for
recruitment of larch regeneration (Kharuk et al. 2013). During range
expansion and reconnection of refugia or at contact areas, hybrids form
and the tendency for this process to occur is common in many forest tree
species and is known for Siberian larch species (Semerikov et al. 2007).
4.3 Absence of northern refugia could possibly explain the current
treeline migration lag
The refugial populations may have served as a starting point for rapid
colonization of the areas north of the treeline in the early Holocene
(Tarasov et al. 2009; Epp et al. 2018). This explains the existence ofLarix in the far north at that time (Bigelow 2003), although the
migration rates at the treelines were slow. Today the initial situation
is different. The climate cooling during the Little Ice Age (LIA;
extending from the 16th to the 19thcenturies) negatively impacted tree population densities and caused
range contraction, while the enhanced recruitment in the twentieth
century has not been of sufficient magnitude to compensate for this
range contraction (MacDonald et al. 2008). As a result, there are
currently no refugial populations in northern Siberia, as was most
likely the case in the early Holocene. This fact could possibly explain
why the current treeline advance is lagging behind climate warming.
However, if individual trees establish themselves in the tundra area
ahead of the treeline in the future, they could be the initial spark for
rapid dispersal of the boreal coniferous forest. If the progressive
forest expansion keeps pace with climate change in the future, as
various studies assume (MacDonald et al. 2008; Pearson et al. 2013;
Kruse and Herzschuh 2022), the habitats of tundra are threatened and
could recede or disappear completely. This knowledge can be implemented
in simulation models such as LAVESI (Larix vegetation simulator)
(Kruse et al. 2016; 2019).
5 Conclusions and outlook
We inferred spatial distribution patterns of the genetic variability of
Siberian larches by GBS. The data are best explained by three and four
genetic groups. However, from an ecological point of view, a
differentiation of five to six clusters has the potential to reveal
admixture regions and not just the main areas in the given region but
even, for example, the emergence of two clusters belonging to the same
species but differing from one another. According to Bobrov’s taxonomic
system (1972), the four statistically verified main clusters match well
with the expected distinction into the three Siberian larch speciesL. sibirica , L. gmelinii, and L. cajanderi from
Western to Eastern Eurasia. The most eastern cluster is in Chukotka and
seems to be another aggregation of L. cajanderi . Furthermore, the
geographical barriers correspond to the habitat zones of the different
species.
Our aim was to answer the question of whether refugia existed in
northern areas during the LGM and to get an idea of the temporal
classification concerning possible demographic events. Altogether the
ABC supports a scenario whereby the present Siberian larch populations
have survived the LGM in refugia in the north, rather than migrating in
the postglacial from the south. The presence of northern LGM refugia may
explain the early existence of larches in the far north in the Holocene
and their dominance until today. In contrast to the past situation,
there are no northern refugia today, which could delay the treeline
advance to the north despite climate warming.
The results of this study provide a better understanding on how refugial
populations contribute to the treeline migration of Siberian larches.
Furthermore, cluster analysis could be used to search for possible
refugial populations on a small scale for conservation purposes.
Additionally, more complex scenarios, complementary to the most probable
scenario detected in the present study, could be analyzed using the ABC
method.
References
Abaimov, A. P. (2010). Geographical distribution and genetics of
Siberian larch species. In A. Osawa, O. A. Zyryanova, Y. Matsuura, T.
Kajimoto, & R. W. Wein (Eds.), Permafrost ecosystems: Siberian larch
forests (Ecological Studies Vol. 209, pp. 41–58). Springer, Dordrecht.
https://doi.org/10.1007/978-1-4020-9693-8_3
Andreev, A. A., Nazarova, L. B., Lenz, M. M., Böhmer, T., Syrykh, L.,
Wagner, B., Melles, M., Pestryakova, L. A., & Herzschuh, U. (2022).
Late Quaternary paleoenvironmental reconstructions from sediments of
Lake Emanda (Verkhoyansk Mountains, East Siberia). Journal of Quaternary
Science, 37(5), 884–899. https://doi.org/10.1002/jqs.3419
Andreev, A. A., Schirrmeister, L., Tarasov, P. E., Ganopolski, A.,
Brovkin, V., Siegert, C., Wetterich, S., & Hubberten, H.-W. (2011).
Vegetation and climate history in the Laptev Sea region (Arctic Siberia)
during Late Quaternary inferred from pollen records. Quaternary Science
Reviews, 30(17–18), 2182–2199.
https://doi.org/10.1016/j.quascirev.2010.12.026
Araki, N. H. T., Khatab, I. A., Hemamali, K. K. G. U., Inomata, N.,
Wang, X.-R., & Szmidt, A. E. (2008). Phylogeography of Larix
sukaczewii Dyl. and Larix sibirica L. inferred from nucleotide
variation of nuclear genes. Tree Genetics & Genomes, 4(4), 611–623.
https://doi.org/10.1007/s11295-008-0137-1
Baltunis, B. S., Greenwood, M. S., & Eysteinsson, T. (1998). Hybrid
vigor in Larix : Growth of intra- and interspecific hybrids ofLarix decidua , L. laricina , and L. kaempferi after
5 years. Silvae Genetica, 47(5–6), 288–293.
Bennett, K., & Provan, J. (2008). What do we mean by ‘refugia’?
Quaternary Science Reviews, 27(27–28), 2449–2455.
https://doi.org/10.1016/j.quascirev.2008.08.019
Bigelow, N. H. (2003). Climate change and Arctic ecosystems: 1.
Vegetation changes north of 55°N between the last glacial maximum,
mid-Holocene, and present. Journal of Geophysical Research, 108(D19),
8170. https://doi.org/10.1029/2002JD002558
Binney, H. A., Willis, K. J., Edwards, M. E., Bhagwat, S. A., Anderson,
P. M., Andreev, A. A., Blaauw, M., Damblon, F., Haesaerts, P., Kienast,
F., Kremenetski, K. V., Krivonogov, S. K., Lozhkin, A. V., MacDonald, G.
M., Novenko, E. Y., Oksanen, P., Sapelko, T. V., Väliranta, M., &
Vazhenina, L. (2009). The distribution of late-Quaternary woody taxa in
northern Eurasia: Evidence from a new macrofossil database. Quaternary
Science Reviews, 28(23–24), 2445–2464.
https://doi.org/10.1016/j.quascirev.2009.04.016
Binney, H. A., Edwards, M. E., Macias-Fauria, M., Lozhkin, A., Anderson,
P., Kaplan, J. O., Andreev, A., Bezrukova, E., Blyakharchuk, T.,
Jankovska, V., Khazina, I., Krivonogov, S., Kremenetski, K., Nield, J.,
Novenko, E. Y., Ryabogina, N., Solovieva, N., Willis, K. J., &
Zernitskaya, V. (2017). Vegetation of Eurasia from the last glacial
maximum to present: Key biogeographic patterns. Quaternary Science
Reviews, 157, 80–97. https://doi.org/10.1016/j.quascirev.2016.11.022
Bobrov, E. G. (1972). History and systematics of Larix . Journal
of Botany, 60(6), 797–805.
Bonan, G. B. (2008). Forests and climate change: Forcings, feedbacks,
and the climate benefits of forests. Science, 320(5882), 1444–1449.
https://doi.org/10.1126/science.1155121
Borsch, T., Berendsohn, W., Dalcin, E., Delmas, M., Demissew, S.,
Elliott, A., Fritsch, P., Fuchs, A., Geltman, D., Güner, A., Haevermans,
T., Knapp, S., Roux, M. M., Loizeau, P., Miller, C., Miller, J., Miller,
J. T., Palese, R., Paton, A., … Zamora, N. (2020). World Flora
Online: Placing taxonomists at the heart of a definitive and
comprehensive global resource on the world’s plants. TAXON, 69(6),
1311–1341. https://doi.org/10.1002/tax.12373
Brubaker, L. B., Anderson, P. M., Edwards, M. E., & Lozhkin, A. V.
(2005). Beringia as a glacial refugium for boreal trees and shrubs: new
perspectives from mapped pollen data. Journal of Biogeography, 32(5),
833–848. https://doi.org/10.1111/j.1365-2699.2004.01203.x
Cao, X., Tian, F., Andreev, A., Anderson, P. M., Lozhkin, A. V.,
Bezrukova, E., Ni, J., Rudaya, N., Stobbe, A., Wieczorek, M., &
Herzschuh, U. (2020). A taxonomically harmonized and temporally
standardized fossil pollen dataset from Siberia covering the last 40
kyr. Earth System Science Data, 12(1), 119–135.
https://doi.org/10.5194/essd-12-119-2020
Cao, X., Tian, F., Li, F., Gaillard, M.-J., Rudaya, N., Xu, Q., &
Herzschuh, U. (2019). Pollen-based quantitative land-cover
reconstruction for northern Asia covering the last 40 ka cal BP. Climate
of the Past, 15(4), 1503–1536. https://doi.org/10.5194/cp-15-1503-2019
Chen, C., Mitchell, S. E., Elshire, R. J., Buckler, E. S., &
El-Kassaby, Y. A. (2013). Mining conifers’ mega-genome using rapid and
efficient multiplexed high-throughput genotyping-by-sequencing (GBS) SNP
discovery platform. Tree Genetics & Genomes, 9(6), 1537–1544.
https://doi.org/10.1007/s11295-013-0657-1
Cornuet, J.-M., Pudlo, P., Veyssier, J., Dehne-Garcia, A., Gautier, M.,
Leblois, R., Marin, J.-M., & Estoup, A. (2014). DIYABC v2.0: A software
to make approximate Bayesian computation inferences about population
history using single nucleotide polymorphism, DNA sequence and
microsatellite data. Bioinformatics, 30(8), 1187–1189.
https://doi.org/10.1093/bioinformatics/btt763
Deschamps, S., Llaca, V., & May,
G. D. (2012). Genotyping-by-Sequencing in Plants. Biology, 1(3),
460–483. https://doi.org/10.3390/biology1030460
Dong, M., He, Q., Zhao, J., Zhang, Y., Yuan, D., & Zhang, J. (2019).
Genetic Mapping of Prince Rupprecht’s Larch (Larix
principis-rupprechtii Mayr) by Specific-Locus Amplified Fragment
Sequencing. Genes, 10(8), 583. https://doi.org/10.3390/genes10080583
Dylis, N. V. (1961). Larch species of East Siberia and the Far East. AN
SSSR, Moscow, 209.
Eaton, D. A. R., & Overcast, I. (2020). ipyrad: Interactive assembly
and analysis of RADseq datasets. Bioinformatics, 36(8), 2592–2594.
https://doi.org/10.1093/bioinformatics/btz966
Eckert, A. J., Bower, A. D., González-Martínez, S. C., Wegrzyn, J. L.,
Coop, G., & Neale, D. B. (2010). Back to nature: Ecological genomics of
loblolly pine (Pinus taeda , Pinaceae). Molecular Ecology, 19(17),
3789–3805. https://doi.org/10.1111/j.1365-294X.2010.04698.x
Epp, L. S., Kruse, S., Kath, N. J., Stoof-Leichsenring, K. R.,
Tiedemann, R., Pestryakova, L. A., & Herzschuh, U. (2018). Temporal and
spatial patterns of mitochondrial haplotype and species distributions in
Siberian larches inferred from ancient environmental DNA and modeling.
Scientific Reports, 8(1), 17436.
https://doi.org/10.1038/s41598-018-35550-w
Francois, O. (2016). Running Structure-like Population Genetic Analyses
with R. University of Grenoble-Alpes, 1–8.
Franz, H. J. (1973). Physische Geographie der Sowjetunion. Haack.
Freeland, J. R. (2020). Molecular ecology. John Wiley & Sons.
Frichot, E., & François, O. (2015). LEA: An R package for landscape and
ecological association studies. Methods in Ecology and Evolution, 6(8),
925–929. https://doi.org/10.1111/2041-210X.12382
Frichot, E., Mathieu, F., Trouillon, T., Bouchard, G., & François, O.
(2014). Fast and efficient estimation of individual ancestry
coefficients. Genetics, 196(4), 973–983.
https://doi.org/10.1534/genetics.113.160572
Harsch, M. A., Hulme, P. E., McGlone, M. S., & Duncan, R. P. (2009).
Are treelines advancing? A global meta-analysis of treeline response to
climate warming. Ecology Letters, 12(10), 1040–1049.
https://doi.org/10.1111/j.1461-0248.2009.01355.x
Herzschuh, U. (2020). Legacy of the Last Glacial on the present‐day
distribution of deciduous versus evergreen boreal forests. Global
Ecology and Biogeography, 29(2), 198–206.
https://doi.org/10.1111/geb.13018
Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages.
Nature, 405(6789), 907–913. https://doi.org/10.1038/35016000
Holtmeier, F. K., & Broll, G. E. (2007). Treeline advance—Driving
processes and adverse factors. Landscape Online, 1, 1–33.
https://doi.org/10.3097/LO.200701
IPCC (2022). Climate Change 2022: Impacts, Adaptation and Vulnerability.
Contribution of Working Group II to the Sixth Assessment Report of the
Intergovernmental Panel on Climate Change [H.-O. Pörtner, D.C.
Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M.
Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, B. Rama (eds.)].
Cambridge University Press. Cambridge University Press, Cambridge, UK
and New York, NY, USA, 3056 pp., https://doi.org/10.1017/9781009325844.
Isaev, A. P., Protopopov, A. V., Protopopova, V. V., Egorova, A. A.,
Timofeyev, P. A., Nikolaev, A. N., Shurduk, I.F., Lytkina, L.P.,
Ermakov, N.B., Nikitina, N.V., Efimova, A.P., Zakharova, V.I., Cherosov,
M.M., Nikolin, E.G., Sosina, N.K., Troeva, E.I., Gogoleva, P.A.,
Kuznetsova, L.V., Pestryakov, B.N., Mironova, S.I., and Sleptsova, N. P.
(2010). Vegetation of Yakutia: elements of ecology and plant sociology.
In E. I. Troeva, A. P. Isaev, M. M. Cherosov, & N. S. Karpov (Eds) The
Far North: plant biodiversity and ecology of Yakutia (pp. 143–260),
Springer. https://doi.org/10.1007/978-90-481-3774-9_3
Johnson, J., Chhetri, P., Krutovsky, K., & Cairns, D. (2017). Growth
and its relationship to individual genetic diversity of Mountain Hemlock
(Tsuga mertensiana ) at alpine treeline in Alaska: combining
dendrochronology and genomics. Forests, 8(11), 418.
https://doi.org/10.3390/f8110418
Kajimoto, T. (2010). Root system development of larch trees growing on
Siberian permafrost. In A. Osawa, O. A. Zyryanova, Y. Matsuura, T.
Kajimoto, & R. W. Wein (Eds.), Permafrost ecosystems: Siberian larch
forests (Ecological Studies Vol. 209, pp. 303–330), Springer,
Dordrecht. https://doi.org/10.1007/978-1-4020-9693-8_16
Kharuk, V. I., Ranson, K. J., Im, S. T., Oskorbin, P. A., Dvinskaya, M.
L., & Ovchinnikov, D. V. (2013). Tree-line structure and dynamics at
the northern limit of the larch forest: Anabar Plateau, Siberia, Russia.
Arctic, Antarctic, and Alpine Research, 45(4), 526–537.
https://doi.org/10.1657/1938-4246-45.4.526
Khatab, I. A., Ishiyama, H., Inomata, N., Wang, X.-R., & Szmidt, A. E.
(2008). Phylogeography of Eurasian Larix species inferred from
nucleotide variation in two nuclear genes. Genes & Genetic Systems,
83(1), 55–66. https://doi.org/10.1266/ggs.83.55
Kruse, S., Gerdes, A., Kath, N. J., Epp, L. S., Stoof-Leichsenring, K.
R., Pestryakova, L. A., & Herzschuh, U. (2019). Dispersal distances and
migration rates at the arctic treeline in Siberia – a genetic and
simulation-based study. Biogeosciences, 16(6), 1211–1224.
https://doi.org/10.5194/bg-16-1211-2019
Kruse, S., Gerdes, A., Kath, N. J., & Herzschuh, U. (2018).
Implementing spatially explicit wind-driven seed and pollen dispersal in
the individual-based larch simulation model: LAVESI-WIND 1.0.
Geoscientific Model Development, 11(11), 4451–4467.
https://doi.org/10.5194/gmd-11-4451-2018
Kruse, S., & Herzschuh, U. (2022). Regional opportunities for tundra
conservation in the next 1000 years. ELife, 11, e75163.
https://doi.org/10.7554/eLife.75163
Kruse, S., Wieczorek, M., Jeltsch, F., & Herzschuh, U. (2016). Treeline
dynamics in Siberia under changing climates as inferred from an
individual-based model for Larix . Ecological Modelling, 338,
101–121. https://doi.org/10.1016/j.ecolmodel.2016.08.003
LePage, B. A., & Basinger, J. F. (1995). The evolutionary history of
the genus Larix (Pinaceae). U.S. Department of Agriculture,
Forest Service, Intermountain Research Station, GTR-INT-31 (pp.
19–219).
Li, Y., Zhang, X., & Fang, Y. (2019). Landscape features and climatic
forces shape the genetic structure and evolutionary history of an oak
species (Quercus chenii ) in East China. Frontiers in Plant
Science, 10, 1060. https://doi.org/10.3389/fpls.2019.01060
Lozhkin, A., Anderson, P., Minyuk, P., Korzun, J., Brown, T., Pakhomov,
A., Tsygankova, V., Burnatny, S., & Naumov, A. (2018). Implications for
conifer glacial refugia and postglacial climatic variation in western
Beringia from lake sediments of the Upper Indigirka basin. Boreas,
47(3), 938–953. https://doi.org/10.1111/bor.12316
Ma, L., Cao, L., Hoffmann, A. A., Gong, Y., Chen, J., Chen, H., Wang,
X., Zeng, A., Wei, S., & Zhou, Z. (2020). Rapid and strong population
genetic differentiation and genomic signatures of climatic adaptation in
an invasive mealybug. Diversity and Distributions, 26(5), 610–622.
https://doi.org/10.1111/ddi.13053
MacDonald, G. M., Kremenetski, K. V., & Beilman, D. W. (2008). Climate
change and the northern Russian treeline zone. Philosophical
Transactions of the Royal Society B: Biological Sciences, 363(1501),
2283–2299. https://doi.org/10.1098/rstb.2007.2200
MacDonald, G. M., Velichko, A. A., Kremenetski, C. V., Borisova, O. K.,
Goleva, A. A., Andreev, A. A., Cwynar, L. C., Riding, R. T., Forman, S.
L., Edwards, T. W. D., Aravena, R., Hammarlund, D., Szeicz, J. M., &
Gattaulin, V. N. (2000). Holocene treeline history and climate change
across northern Eurasia. Quaternary Research, 53(3), 302–311.
https://doi.org/10.1006/qres.1999.2123
Müller, S., Tarasov, P. E., Andreev, A. A., Tütken, T., Gartz, S., &
Diekmann, B. (2010). Late Quaternary vegetation and environments in the
Verkhoyansk Mountains region (NE Asia) reconstructed from a 50-kyr
fossil pollen record from Lake Billyakh. Quaternary Science Reviews,
29(17–18), 2071–2086. https://doi.org/10.1016/j.quascirev.2010.04.024
Mayr, H. (1906). Fremdländische Wald-und Parkbäume für Europa. P. Parey.
Napier, J. D., Fernandez, M. C., de Lafontaine, G., & Hu, F. S. (2020).
Ice‐age persistence and genetic isolation of the disjunct distribution
of larch in Alaska. Ecology and Evolution, 10(3), 1692–1702.
Pearson, R. G., Phillips, S. J., Loranty, M. M., Beck, P. S. A.,
Damoulas, T., Knight, S. J., & Goetz, S. J. (2013). Shifts in Arctic
vegetation and associated feedbacks under climate change. Nature Climate
Change, 3(7), 673–677. https://doi.org/10.1038/nclimate1858
Petit, R. J., Duminil, J., Fineschi, S., Hampe, A., Salvini, D., &
Vendramin, G. G. (2004). Comparative organization of chloroplast,
mitochondrial and nuclear diversity in plant populations. Molecular
Ecology, 14(3), 689–701.
https://doi.org/10.1111/j.1365-294X.2004.02410.x
Polezhaeva, M. A., Lascoux, M., & Semerikov, V. L. (2010). Cytoplasmic
DNA variation and biogeography of Larix Mill. in northeast Asia.
Molecular Ecology, 19(6), 1239–1252.
https://doi.org/10.1111/j.1365-294X.2010.04552.x
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R.,
Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., &
Sham, P. C. (2007). PLINK: A tool set for whole-genome association and
population-based linkage analyses. The American Journal of Human
Genetics, 81(3), 559–575. https://doi.org/10.1086/519795
Railsback, L. B. (2006). Some fundamentals of mineralogy and
geochemistry. On-line book, quoted from:
http://railsback.org/FundamentalsIndex.html.
Rousset, F. (1999). Genetic differentiation within and between two
habitats. Genetics, 151(1), 397–407.
https://doi.org/10.1093/genetics/151.1.397
Rowe, G., Sweet, M., & Beebee, T. J. C. (2017). An Introduction to
Molecular Ecology. Oxford University Press.
Schnell, R. J., & Priyadarshan, P. M. (Eds.). (2012). Genomics of Tree
Crops. Springer Science & Business Media.
Schulte, L., Bernhardt, N., Stoof‐Leichsenring, K. R., Zimmermann, H.
H., Pestryakova, L. A., Epp, L. S., & Herzschuh, U. (2021).
Hybridization capture of larch (Larix Mill.) chloroplast genomes
from sedimentary ancient DNA reveals past changes of Siberian forest.
Molecular Ecology Resources, 21(3), 801–815.
https://doi.org/10.1111/1755-0998.13311
Schulte, L., Li, C., Lisovski, S., & Herzschuh, U. (2022a).
Forest‐permafrost feedbacks and glacial refugia help explain the unequal
distribution of larch across continents. Journal of Biogeography,
49(10), 1825–1838. https://doi.org/10.1111/jbi.14456
Schulte, L., Meucci, S., Stoof-Leichsenring, K. R., Heitkam, T.,
Schmidt, N., Von Hippel, B., Andreev, A. A., Diekmann, B., Biskaborn, B.
K., Wagner, B., Melles, M., Pestryakova, L. A., Alsos, I. G., Clarke,
C., Krutovsky, K. V., & Herzschuh, U. (2022b). Larix species
range dynamics in Siberia since the Last Glacial captured from
sedimentary ancient DNA. Communications Biology, 5(1), 570.
https://doi.org/10.1038/s42003-022-03455-0
Semerikov, V. L., Iroshnikov, A. I., & Lascoux, M. (2007).
Mitochondrial DNA variation pattern and postglacial history of the
Siberian larch (Larix sibirica Ledeb.). Russian Journal of
Ecology, 38(3), 147–154. https://doi.org/10.1134/S1067413607030010
Semerikov, V. L., Semerikov, L. F., & Lascoux, M. (1999). Intra- and
interspecific allozyme variability in Eurasian Larix Mill.
species. Heredity, 82(2), 193–204.
https://doi.org/10.1038/sj.hdy.6884710
Semerikov, V. L., Semerikova, S. A., Polezhaeva, M. A., Kosintsev, P.
A., & Lascoux, M. (2013). Southern montane populations did not
contribute to the recolonization of West Siberian Plain by Siberian
larch (Larix sibirica ): A range-wide analysis of cytoplasmic
markers. Molecular Ecology, 22(19), 4958–4971.
https://doi.org/10.1111/mec.12433
Smith, D. R. (2015). Mutation rates in plastid genomes: they are lower
than you might think. Genome Biology and Evolution, 7(5), 1227–1234.
https://doi.org/10.1093/gbe/evv069
Stewart, J. R., & Lister, A. M. (2001). Cryptic northern refugia and
the origins of the modern biota. Trends in Ecology & Evolution, 16(11),
608–613. https://doi.org/10.1016/S0169-5347(01)02338-2
Szafer, W. (1913). Contribution to the knowledge of Eurasian larch
species with particular attention paid to larch species occurring in
Poland. Kosmos 38: 1021, 1281–1315 (in Polish).
Tarasov, P., Müller, S., Andreev, A., Werner, K., & Diekmann, B.
(2009). Younger Dryas Larix in eastern Siberia: A migrant or
survivor? PAGES News, 17(3), 122–123.
https://doi.org/10.22498/pages.17.3.122
Tóth, E. G., Tremblay, F., Housset, J. M., Bergeron, Y., & Carcaillet,
C. (2019). Geographic isolation and climatic variability contribute to
genetic differentiation in fragmented populations of the long-lived
subalpine conifer Pinus cembra L. in the western Alps. BMC
Evolutionary Biology, 19(1), 190.
https://doi.org/10.1186/s12862-019-1510-4
Tsumura, Y., Kimura, M., Nakao, K., Uchiyama, K., Ujino-Ihara, T., Wen,
Y., Tong, Z., & Han, W. (2020). Effects of the last glacial period on
genetic diversity and genetic differentiation in Cryptomeria
japonica in East Asia. Tree Genetics & Genomes, 16(1), 19.
https://doi.org/10.1007/s11295-019-1411-0
Väliranta, M., Kaakinen, A., Kuhry, P., Kultti, S., Salonen, J. S., &
Seppä, H. (2011). Scattered late-glacial and early Holocene tree
populations as dispersal nuclei for forest development in north-eastern
European Russia: Holocene forest development in north-eastern European
Russia. Journal of Biogeography, 38(5), 922–932.
https://doi.org/10.1111/j.1365-2699.2010.02448.x
Wendler, N., Mascher, M., Nöh, C., Himmelbach, A., Scholz, U.,
Ruge‐Wehling, B., & Stein, N. (2014). Unlocking the secondary gene‐pool
of barley with next‐generation sequencing. Plant Biotechnology Journal,
12(8), 1122–1131.
Zhang, N., Yasunari, T., & Ohta, T. (2011). Dynamics of the larch
taiga–permafrost coupled system in Siberia under climate change.
Environmental Research Letters, 6(2), 024003.
https://doi.org/10.1088/1748-9326/6/2/024003
Zhang, W., Miller, P. A., Smith, B., Wania, R., Koenigk, T., & Döscher,
R. (2013). Tundra shrubification and tree-line advance amplify arctic
climate warming: Results from an individual-based dynamic vegetation
model. Environmental Research Letters, 8(3), 034023.
https://doi.org/10.1088/1748-9326/8/3/034023