1 Introduction
The
extensive forests in East Siberia
are dominated by deciduous larch species (Larix spp.). These
unique forests mostly grow on continuous permafrost, to which the
larches with their shallow roots are well adapted (Kajimoto 2009). The
larches also stabilize the permafrost (Zhang et al. 2011). Changing
climate forces species worldwide to migrate (Pearson et al. 2013) and
exceptional attention is paid to the high northern latitudes since
climate change here is faster and more severe than in other regions
(IPCC 2022). Siberian boreal forests are expected to expand northwards
in the course of modern global warming (MacDonald et al. 2008; Andreev
et al. 2011). This tundra-taiga transition will be accompanied by an
albedo decrease, which in turn will raise regional temperatures (Bonan
2008). This additional warming can offset the negative forcing that is
expected from carbon sequestration (Zhang et al. 2013). However, the
processes of the treeline ecotone transition that would lead to
different climate feedbacks, as well as timing are still poorly
understood.
The
speed and spatial pattern of a species’ response to climate change are
determined by several processes. The biogeographic history of larches
(Larix ssp.) in Eurasia has been predominantly shaped by the
alternating glacial and interglacial periods over the last three million
years (Hewitt 2000). The trees
either persisted in northern refugia or they survived in southern areas
under less harsh climatic conditions from where they invaded in the
postglacial (Bennett and Provan 2008).
Relict forest stands of past warm
phases which have survived in refugia ahead of the current treeline can
speed up the migration rate of treelines estimated from observational
studies (Stewart and Lister 2001; Holtmeier and Broll 2007; MacDonald et
al. 2008; Väliranta et al. 2011) and modelling (Kruse et al. 2019). In
line with these general findings, radiocarbon-dated macrofossil findings
suggest a fast range expansion of the boreal Larix forests at the
end of the Late Glacial and the beginning of the Holocene (MacDonald et
al. 2000; Andreev et al. 2022). However, modeling current responses of
the Siberian larch forest reveals that tree stands respond with a
pronounced time lag to the current climate change (Kruse et al. 2016).
To predict the future climate response under the current global warming,
we need more reliable estimates of species range expansion rates to
implement in simulation models. Therefore, knowledge about the influence
of relict trees from an earlier wider extent of the forest on migration
dynamics is of great importance.
Fossil records of Larix show that the genus became a
well-established forest constituent in northeastern Russia by the late
Oligocene (26.5 to 24 mya) (LePage and Basinger 1995). Recent Siberian
larch species, especially L. gmelinii , probably formed as an
adaptation to the increasing climatic continentality in the Pleistocene
(Abaimov 2010). Larix formed forests in Siberia throughout the
Holocene (Cao et al. 2019). Several paleoecological studies indicate the
existence of refugia for Larix in northern areas during the
coldest phases of the latest Pleistocene, particularly the Last Glacial
Maximum (LGM; approximately 21,000 years BP), even when there was very
likely a relatively low density of larch (Cao et al. 2020). Pollen and
macrofossil records suggest that local Larix populations
persisted in northern Asia in general (Schulte et al. 2022a) and within
western Beringia (Brubaker et al. 2005; Lozhkin et al. 2018), in the
western foreland of the Verkhoyansk Mountains (Tarasov et al. 2009;
Müller et al. 2010), and even on the Taymyr Peninsula (Binney et al.
2009). However, although these previous studies reveal examples of
Siberian refugial populations that persisted during the LGM, it remains
unclear as to what extent and how these Siberian glacial refugial
populations genetically contributed to postglacial recolonization and
the modern genetic pool.
Genetic analyses have been used
to reveal local dispersal patterns and population genetics and to infer
the historical biogeography of the larches in Siberia (Herzschuh 2020).
Araki et al. (2008) suggest that the investigated Larix
sukaczewii and L. sibirica populations were founded by migrants
from multiple, genetically distinct refugia. Semerikov et al. (1999;
2013) conducted one of the few species-wide population genetic studies
of L. sibirica , and reveal, using cytoplasmic markers, that the
southernmost populations of L. sibirica had a very limited
contribution to the current populations of the central and northern
parts of its range. In contrast, a recent study was able to distinguish
between L. sibirica and L. gmelinii in glacial refugial
populations by enriching sedimentary ancient DNA extracts for
chloroplast genome sequences (Schulte et al. 2021; Schulte et al.
2022b). These studies reveal that northern refugial populations existed
during the LGM and were almost exclusively composed of L.
gmelinii . Larix sibirica , on the other hand, recolonized from
southern refugia. However, for the vast distribution area of larches in
Eastern Siberia and the other Siberian larch species the knowledge is
very limited.
The genetic markers previously
used to study phylogeography were limited to a few informal sequences
and mostly localized to plastids. This limitation can be overcome by the
recently developed approach of genotyping by sequencing (GBS) that
enables the analysis of hundreds to thousands of nuclear loci at a low
cost and gives deep insights into their phylogeography as well as
adaptation. GBS combines complexity reduction, multiplexing of samples,
and the use of next-generation sequencing (NGS) methods for genotyping
of whole mapping populations (Wendler et al. 2014) and is feasible for
high diversity, large genome species such as larches (Larix spp.)
(Elshire et al. 2011). In addition, the analysis of nuclear DNA has
other advantages, as it contains complementary information to plastid
DNA due to different modes of inheritance (Petit et al. 2004). Many
gymnosperms inherit plastid DNA from male pollen which is spread in the
wind and mitochondrial DNA is normally inherited exclusively from the
mother (Freeland 2005). Additionally, for land plants, the plastid and
nuclear genomes have an ∼3- to 10-fold greater mutation rate than the
mitochondrial genome (Smith 2015). Thus, we could expect to detect
higher levels of genetic structure among populations using biparentally
inherited nuclear DNA from the GBS analyses. To our knowledge, GBS has
not yet been used to infer population structures and hence unravel the
biogeography of larches (Larix Mill.).
The overall aim of this study is to provide a better understanding of
the importance of glacial relict trees ahead of the treeline on the
postglacial migration rate of Siberian larches across the continent.
Therefore, we examine genecological interrelations of representatively
sampled populations across Eastern Siberia (Larix sibiricaLedeb., L. gmelinii (Rupr) Rupr., L. cajanderi Mayr.)
using single nucleotide polymorphisms (SNPs) derived by GBS. The
specific objectives are (1) to reveal patterns in the genetic
composition of Siberian larches (Larix spp.) by assessing the
spatial distribution of SNPs using cluster analysis, and (2) to unravel
the potential demographic history to test whether the initiation of the
current populations can be dated before the Last Glacial Maximum (LGM).