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).