High resolution ancient sedimentary DNA shows that alpine plant diversity is associated with human land use and climate change

Article https://doi.org/10.1038/s41467-022-34010-4 High resolution ancient sedimentary DNA shows that alpine plant diversity is associated with human land use and climate change Received: 15 September 2021 1234567890():,; 1234567890():,; Accepted: 6 October 2022 Check for updates Sandra Garcés-Pastor 1 , Eric Coissac 2, Sébastien Lavergne2, Christoph Schwörer 3, Jean-Paul Theurillat 4, Peter D. Heintzman1, Owen S. Wangensteen 5,6, Willy Tinner3, Fabian Rey7, Martina Heer7, Astrid Rutzer7, Kevin Walsh 8, Youri Lammers 1, Antony G. Brown1, Tomasz Goslar 9, Dilli P. Rijal 1, Dirk N. Karger 10, Loïc Pellissier 11,12, The PhyloAlps Consortium*, Oliver Heiri 7,29 & Inger Greve Alsos 1,29 The European Alps are highly rich in species, but their future may be threatened by ongoing changes in human land use and climate. Here, we reconstructed vegetation, temperature, human impact and livestock over the past ~12,000 years from Lake Sulsseewli, based on sedimentary ancient plant and mammal DNA, pollen, spores, chironomids, and microcharcoal. We assembled a highly-complete local DNA reference library (PhyloAlps, 3923 plant taxa), and used this to obtain an exceptionally rich sedaDNA record of 366 plant taxa. Vegetation mainly responded to climate during the early Holocene, while human activity had an additional influence on vegetation from 6 ka onwards. Land-use shifted from episodic grazing during the Neolithic and Bronze Age to agropastoralism in the Middle Ages. Associated human deforestation allowed the coexistence of plant species typically found at different elevational belts, leading to levels of plant richness that characterise the current high diversity of this region. Our findings indicate a positive association between low intensity agropastoral activities and precipitation with the maintenance of the unique subalpine and alpine plant diversity of the European Alps. Changing environmental conditions are displacing organisms out of their ranges, causing severe threats to biodiversity1. In high mountains, vegetation composition is naturally determined by temperature, moisture, landforms, and geomorphological processes along elevational belts. In addition, many mountain ranges have been under human influence for millennia2, and both natural and anthropogenic forces have shaped the diversity of mountain vegetation3. Climatebased projections indicate an expected upward displacement of vegetation that will reduce habitat for alpine species, while changes in mountain land use with land abandonment in the last century have been causing increasing forest cover and loss of habitat for meadow species3,4. Plant remains in lake sediments allow us to explore vegetation responses to past climate changes and human activity, particularly at long time scales relevant for anticipating future vegetation responses to global changes. Therefore, detailed palaeoecological records representing the full range of plant types and functional A full list of affiliations appears at the end of the paper. *A list of authors and their affiliations appears at the end of the paper. e-mail: Nature Communications | (2022)13:6559 1 Article https://doi.org/10.1038/s41467-022-34010-4 groups that compose alpine and subalpine vegetation are needed to understand how long-term interactions of climate and humans affect overall biodiversity and survival of high elevation plants. However, some ecologically relevant groups such as graminoids and forbs are poorly represented in conventional palaeoecological records due to limited taxonomic resolution and low pollen production, respectively5. Recent advances in sedimentary ancient DNA (sedaDNA) have greatly improved our ability to give detailed insight into past diversity changes6–8. The European Alps are an important plant biodiversity hotspot9, with ~4000 native plant species10 distributed from the warm lowland Colline vegetation belt to the cold alpine Nival belt10, which results from a complex interplay of natural factors over geological timescales. Changes in climatic and environmental conditions in alpine regions brought suitable conditions for plant migration and speciation, resulting in the formation of high numbers of endemics11,12. However, human activities over millennia have modified, favoured and helped to maintain this diversity with the creation of new habitats at the local scale13. Humans have modified the subalpine and alpine landscapes since the Mesolithic, ca. 10 ka (1 ka = 1000 yr ago), by clearing small areas of forest to attract prey for hunting14,15 while the introduction of agropastoral activities during the Neolithic (from 7.5 ka) drove a downward shift of the treelines2,14–16. Humanenvironment interactions in forested and open vegetation types such as the Subalpine zone led to a mosaic of different habitats that include species-rich meadows8,10,15. As a result, future changes in land use might imply a reduction in vegetation diversity of subalpine and alpine landscapes17. For example, the abandonment of highmountain practices during the last half-century has reduced the plant diversity of subalpine pastures in many mountain ranges such B A 50°N 48°N as the European Alps13,18, the Pyrenees19, and the Himalayas20. Understanding the contribution of past climate and land use in shaping alpine vegetation can help anticipate future impacts of global changes and may offer mitigation solutions. Here, we reconstruct the vegetation around Lake Sulsseewli, located in the northern Swiss Alps (Fig. 1), with the aim to better understand the drivers of the species composition and elevational vegetation belts over the past 12,000 years. For this aim, we used a multiproxy approach consisting of plant sedaDNA, pollen, fossil chironomids for summer temperature reconstruction, precipitation data from CHELSA-TraCE21k model21, geochemical proxies, and multiple independent indicators of human activity, that included microscopic charcoal (reflecting fire activity) and grazing indicators (coprophilous fungi spores and mammalian sedaDNA). Based on this comprehensive dataset, we investigated to what extent the current plant richness at Sulsseewli was related to past variations in climate and human activities. To achieve these aims, we assembled trnL P6 loop locus data from a new comprehensive taxonomic DNA reference database consisting of 3923 plant species collected in the Alps and 417 from the Carpathians (the PhyloAlps database; http://phyloalps.org/). The exceptionally high taxonomic resolution of the plant sedaDNA data allowed us to reconstruct both long-term changes in plant diversity and changes in plants that are particularly temperature-sensitive (i.e., with restricted elevational distributions), or are considered pastoral and arable indicators22. Our results suggest that vegetation was mainly driven by climate during the first half of the Holocene (~11 to 6 ka) and that the rise of diversity that characterises the present subalpine and alpine divers (...truncated)