Vegetation changes and treeline dynamics in northern Siberia since the last interglacial revealed by sedimentary ancient DNA metabarcoding and organelle genome assembly of modern larches

heike.zimmermann [ at ]


The arctic-boreal treeline describes the transition zone from taiga to tundra and is a sensitive, climatically driven ecosystem boundary. In Siberia it is formed by deciduous larches as the only representatives of the tree growth form. The recurrent cycles of interglacial and glacial periods throughout the Quaternary resulted in the systematic relocation of the treeline. Awareness of the complex climate-feedback mechanisms of larch forests and their importance for the global carbon cycle is rising. Still, our understanding of genetic variation within and among treeline populations of larches is very limited, as these populations have so far not been focused upon. Patterns of genetic variation in modern populations represent only a snapshot in time, and past climatic changes might have led to a reorganisation of such patterns. Hence, tracing the dynamics of genetic variation in response to climatic changes from the past to the present will improve our perspective on the processes involved in treeline advances and retreats. However, paleobotanic reconstructions rarely date back to the last interglacial (~130-110 kyr BP), as not many locations are known to have preserved suitable deposits. Therefore, our knowledge about the past vegetation and treeline dynamics in northern Siberia predating the Last Glacial Maximum (LGM, ~21-18 kyr BP) is limited. The overall goal of this thesis is to improve our understanding of climatically driven vegetation changes and treeline dynamics since the last interglacial, as well as to provide a baseline for exploring genetic variation in modern and past larch populations from environmental samples. In the scope of this thesis I used sedimentary ancient DNA (sedaDNA) from permafrost sediment cores from the Buor Khaya Peninsula and Bol’shoy Lyakhovsky Island to analyse floristic diversity and composition changes since the last interglacial. In one core, sedaDNA was additionally compared with the pollen record to assess how well sedaDNA reflects past plant community changes. I applied the universal chloroplast trnL-UAA P6-loop marker in a DNA metabarcoding approach, coupled with parallel high-throughput sequencing. Thereafter, I sequenced and assembled 19 paternally inherited chloroplast and maternally inherited mitochondrial genomic references of Larix gmelinii (Rupr.) Rupr. and Larix cajanderi Mayr, which are the two dominant larch species in northern Siberia. The individuals were sampled along the treeline (longitudinal transect) as well as along the ecological gradient, from the single-tree tundra in the north to closed forests in the south (latitudinal transect). This allowed me to identify genetic variation in the form of single nucleotide polymorphisms (SNPs). These SNPs were subsequently used to analyse their modern geographic distribution patterns and to design two chloroplast SNP markers for the analysis of their distribution patterns in prehistoric larch populations from environmental samples. The markers were applied to validate the presence of larch DNA in the ancient permafrost sediment samples. The sedaDNA approach revealed the local floral diversity in high detail, with most taxa resolved to species or genus level. Differences in floral diversity reflected climatically driven environmental changes, generally with the highest level of diversity in warmer, and lower levels in cooler phases. In comparison, the pollen analysis represented the floristic diversity on a regional scale. After the LGM, continuously lower proportions of larch pollen indicate less favourable conditions at the Buor Khaya Peninsula than before the LGM, with regional environmental conditions showing an increase in humidity after the LGM. These observations support the hypothesis that treeline responses to climate warming are geographically heterogeneous and do not necessarily lead to a continuous treeline advance. Treeline transitions were more pronounced at the high arctic, today treeless island Bol’shoy Lyakhovsky than at the Buor Khaya Peninsula. Paleobotanic reconstructions based on sedaDNA revealed a diversity of trees and shrubs during the last interglacial, pointing towards an open, mixed broadleaved, deciduous and evergreen coniferous forest, probably in a spatial mosaic with tundra-steppe. In comparison, the following warm interstadials rather indicate an open, deciduous coniferous forest, probably interspersed by areas of tundra-steppe. A notable observation was the presence of Larix directly after the LGM in the Bølling-Allerød interstadial complex. This supports the hypothesis that larch populations persisted at high latitudes during the LGM, which would have allowed a quick re-colonization of Bol’shoy Lyakhovsky Island. The disappearance of trees and nearly all shrubs from the island took place in the Holocene and was most likely associated with increasingly humid conditions due to the sea level rise and the disconnection of the island from the mainland. A genome-wide comparison of the 19 complete chloroplast genomes resulted in a set of 84 paternally inherited chloroplast SNPs (pollen-transmitted). The generated haplotype network revealed a putative population expansion event at the Southern Taymyr Peninsula. Furthermore, several chloroplast SNP variants were shared across the northern ranges of Larix gmelinii and Larix cajanderi. The resulting pattern suggests incomplete lineage sorting, without any effect of latitude or longitude. Presumably, owing to the partial assembly of the mitochondrial genome combined with the highly efficient repair mechanisms of mitochondrial genomes, only a small number of five maternally inherited mitochondrial SNPs (seed-transmitted) were identified. Out of seven haplotypes, six were retrieved from the Southern Taymyr Peninsula, whereas only two were retrieved from the northern range of Larix cajanderi. The spatially structured pattern points towards a founder effect in the northern range of Larix cajanderi. The newly designed chloroplast SNP markers were successfully applied to the sedaDNA samples. The presence of larch DNA was confirmed in nearly all samples that contained Larix-sequences in the sedaDNA metabarcoding approach. At Bol’shoy Lyakhovsky Island, both SNP variants of each of the applied chloroplast markers were detected in a sample dating to the last interglacial. Furthermore, the spatio-temporal distribution of one SNP variant suggests its dominance in the northern range of Larix cajanderi, at least since the last interglacial. With this thesis, I provided the tools to analyse range-wide genetic variation in modern larch populations. It has also been shown that it is feasible to trace prehistoric genetic variation and its putative reorganisation by using (sedimentary) ancient DNA from a variety of ancient material. Moreover, the new paleobotanic records in north-eastern Siberia improve our understanding of vegetation changes since the last interglacial. This provides an excellent framework for applying, for example, a hybridization capture approach, which allows for the targeted enrichment of complete chloroplast genomes from environmental samples.

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Zimmermann, H. H. (2017): Vegetation changes and treeline dynamics in northern Siberia since the last interglacial revealed by sedimentary ancient DNA metabarcoding and organelle genome assembly of modern larches , PhD thesis, University of Potsdam.

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