A 2-million-year-old ecosystem in Greenland uncovered by environmental DNA.

Late Pliocene and Early Pleistocene epochs 3.6 to 0.8 million years ago1 had climates resembling those forecasted under future warming2. Palaeoclimatic records show strong polar amplification with mean annual temperatures of 11-19 °C above contemporary values3,4. The biological communities inhabiting the Arctic during this time remain poorly known because fossils are rare5. Here we report an ancient environmental DNA6 (eDNA) record describing the rich plant and animal assemblages of the Kap København Formation in North Greenland, dated to around two million years ago. The record shows an open boreal forest ecosystem with mixed vegetation of poplar, birch and thuja trees, as well as a variety of Arctic and boreal shrubs and herbs, many of which had not previously been detected at the site from macrofossil and pollen records. The DNA record confirms the presence of hare and mitochondrial DNA from animals including mastodons, reindeer, rodents and geese, all ancestral to their present-day and late Pleistocene relatives. The presence of marine species including horseshoe crab and green algae support a warmer climate than today. The reconstructed ecosystem has no modern analogue. The survival of such ancient eDNA probably relates to its binding to mineral surfaces. Our findings open new areas of genetic research, demonstrating that it is possible to track the ecology and evolution of biological communities from two million years ago using ancient eDNA.

Larix species range dynamics in Siberia since the Last Glacial captured from sedimentary ancient DNA.

Climate change is expected to cause major shifts in boreal forests which are in vast areas of Siberia dominated by two species of the deciduous needle tree larch (Larix). The species differ markedly in their ecosystem functions, thus shifts in their respective ranges are of global relevance. However, drivers of species distribution are not well understood, in part because paleoecological data at species level are lacking. This study tracks Larix species distribution in time and space using target enrichment on sedimentary ancient DNA extracts from eight lakes across Siberia. We discovered that Larix sibirica, presently dominating in western Siberia, likely migrated to its northern distribution area only in the Holocene at around 10,000 years before present (ka BP), and had a much wider eastern distribution around 33 ka BP. Samples dated to the Last Glacial Maximum (around 21 ka BP), consistently show genotypes of L. gmelinii. Our results suggest climate as a strong determinant of species distribution in Larix and provide temporal and spatial data for species projection in a changing climate.

Tempo and drivers of plant diversification in the European mountain system.

There is still limited consensus on the evolutionary history of species-rich temperate alpine floras due to a lack of comparable and high-quality phylogenetic data covering multiple plant lineages. Here we reconstructed when and how European alpine plant lineages diversified, i.e., the tempo and drivers of speciation events. We performed full-plastome phylogenomics and used multi-clade comparative models applied to six representative angiosperm lineages that have diversified in European mountains (212 sampled species, 251 ingroup species total). Diversification rates remained surprisingly steady for most clades, even during the Pleistocene, with speciation events being mostly driven by geographic divergence and bedrock shifts. Interestingly, we inferred asymmetrical historical migration rates from siliceous to calcareous bedrocks, and from higher to lower elevations, likely due to repeated shrinkage and expansion of high elevation habitats during the Pleistocene. This may have buffered climate-related extinctions, but prevented speciation along elevation gradients as often documented for tropical alpine floras.

Paleoeconomy more than demography determined prehistoric human impact in Arctic Norway.

Population size has increasingly been taken as the driver of past human environmental impact worldwide, and particularly in the Arctic. However, sedimentary ancient DNA (sedaDNA), pollen and archaeological data show that over the last 12,000 years, paleoeconomy and culture determined human impacts on the terrestrial ecology of Arctic Norway. The large Mortensnes site complex (Ceavccageadgi, 70°N) has yielded the most comprehensive multiproxy record in the Arctic to date. The site saw occupation from the Pioneer period (c. 10,000 cal. years BP) with more intensive use from c. 4,200 to 2,000 cal. years BP and after 1,600 cal. years BP. Here, we combine on-site environmental archaeology with a near-site lake record of plant and animal sedaDNA. The rich animal sedaDNA data (42 taxa) and on-site faunal analyses reveal switches in human dietary composition from early-Holocene fish + marine mammals, to mixed marine + reindeer, then finally to marine + reindeer + domesticates (sheep, cattle, pigs), with highest reindeer concentrations in the last millennium. Archaeological evidence suggests these changes are not directly driven by climate or variation in population densities at the site or in the region, but rather are the result of changing socio-economic activities and culture, probably reflecting settlers' origins. This large settlement only had discernable effects on its hinterland in the last 3,600 years (grazing) and more markedly in the last 1,000 years through reindeer keeping/herding and, possibly domestic stock. Near-site sedaDNA can be linked to and validate the faunal record from archaeological excavations, demonstrating that environmental impacts can be assessed at a landscape scale.

Sedimentary ancient DNA shows terrestrial plant richness continuously increased over the Holocene in northern Fennoscandia.

The effects of climate change on species richness are debated but can be informed by the past. Here, we generated a sedimentary ancient DNA dataset covering 10 lakes and applied novel methods for data harmonization. We assessed the impact of Holocene climate changes and nutrients on terrestrial plant richness in northern Fennoscandia. We find that richness increased steeply during the rapidly warming Early Holocene. In contrast to findings from most pollen studies, we show that richness continued to increase thereafter, although the climate was stable, with richness and the regional species pool only stabilizing during the past three millennia. Furthermore, overall increases in richness were greater in catchments with higher soil nutrient availability. We suggest that richness will increase with ongoing warming, especially at localities with high nutrient availability and assuming that human activity remains low in the region, although lags of millennia may be expected.

Metagenomics: A viable tool for reconstructing herbivore diet.

Metagenomics can generate data on the diet of herbivores, without the need for primer selection and PCR enrichment steps as is necessary in metabarcoding. Metagenomic approaches to diet analysis have remained relatively unexplored, requiring validation of bioinformatic steps. Currently, no metagenomic herbivore diet studies have utilized both chloroplast and nuclear markers as reference sequences for plant identification, which would increase the number of reads that could be taxonomically informative. Here, we explore how in silico simulation of metagenomic data sets resembling sequences obtained from faecal samples can be used to validate taxonomic assignment. Using a known list of sequences to create simulated data sets, we derived reliable identification parameters for taxonomic assignments of sequences. We applied these parameters to characterize the diet of western capercaillies (Tetrao urogallus) located in Norway, and compared the results with metabarcoding trnL P6 loop data generated from the same samples. Both methods performed similarly in the number of plant taxa identified (metagenomics 42 taxa, metabarcoding 43 taxa), with no significant difference in species resolution (metagenomics 24%, metabarcoding 23%). We further observed that while metagenomics was strongly affected by the age of faecal samples, with fresh samples outperforming old samples, metabarcoding was not affected by sample age. On the other hand, metagenomics allowed us to simultaneously obtain the mitochondrial genome of the western capercaillies, thereby providing additional ecological information. Our study demonstrates the potential of utilizing metagenomics for diet reconstruction but also highlights key considerations as compared to metabarcoding for future utilization of this technique.

Giant invasive Heracleum persicum: Friend or foe of plant diversity?

The impact of invasion on diversity varies widely and remains elusive. Despite the considerable attempts to understand mechanisms of biological invasion, it is largely unknown whether some communities' characteristics promote biological invasion, or whether some inherent characteristics of invaders enable them to invade other communities. Our aims were to assess the impact of one of the massive plant invaders of Scandinavia on vascular plant species diversity, disentangle attributes of invasible and noninvasible communities, and evaluate the relationship between invasibility and genetic diversity of a dominant invader. We studied 56 pairs of Heracleum persicum Desf. ex Fisch.-invaded and noninvaded plots from 12 locations in northern Norway. There was lower native cover, evenness, taxonomic diversity, native biomass, and species richness in the invaded plots than in the noninvaded plots. The invaded plots had nearly two native species fewer than the noninvaded plots on average. Within the invaded plots, cover of H. persicum had a strong negative effect on the native cover, evenness, and native biomass, and a positive association with the height of the native plants. Plant communities containing only native species appeared more invasible than those that included exotic species, particularly H. persicum. Genetic diversity of H. persicum was positively correlated with invasibility but not with community diversity. The invasion of a plant community by H. persicum exerts consistent negative pressure on vascular plant diversity. The lack of positive correlation between impacts and genetic diversity of H. persicum indicates that even a small founder population may cause high impact. We highlight community stability or saturation as an important determinant of invasibility. While the invasion by H. persicum may decrease susceptibility of a plant community to further invasion, it severely reduces the abundance of native species and makes them more vulnerable to competitive exclusion.

Fungi Sailing the Arctic Ocean: Speciose Communities in North Atlantic Driftwood as Revealed by High-Throughput Amplicon Sequencing.

High amounts of driftwood sail across the oceans and provide habitat for organisms tolerating the rough and saline environment. Fungi have adapted to the extremely cold and saline conditions which driftwood faces in the high north. For the first time, we applied high-throughput sequencing to fungi residing in driftwood to reveal their taxonomic richness, community composition, and ecology in the North Atlantic. Using pyrosequencing of ITS2 amplicons obtained from 49 marine logs, we found 807 fungal operational taxonomic units (OTUs) based on clustering at 97 % sequence similarity cut-off level. The phylum Ascomycota comprised 74 % of the OTUs and 20 % belonged to Basidiomycota. The richness of basidiomycetes decreased with prolonged submersion in the sea, supporting the general view of ascomycetes being more extremotolerant. However, more than one fourth of the fungal OTUs remained unassigned to any fungal class, emphasising the need for better DNA reference data from the marine habitat. Different fungal communities were detected in coniferous and deciduous logs. Our results highlight that driftwood hosts a considerably higher fungal diversity than currently known. The driftwood fungal community is not a terrestrial relic but a speciose assemblage of fungi adapted to the stressful marine environment and different kinds of wooden substrates found in it.

Reconstructing the invasion history of Heracleum persicum (Apiaceae) into Europe.

Sparse, incomplete and inappropriate historical records of invasive species often hamper invasive species management interventions. Population genetic analyses of invaders might provide a suitable context for the identification of their source populations and possible introduction routes. Here, we describe the population genetics of Heracleum persicum Desf. ex Fisch and trace its route of introduction into Europe. Microsatellite markers revealed a significantly higher genetic diversity of H. persicum in its native range, and the loss of diversity in the introduced range may be attributed to a recent genetic bottleneck. Bayesian cluster analysis on regional levels identified three and two genetic clusters in the native and the introduced ranges, respectively. A global structure analysis revealed two worldwide distinct genetic groups: one primarily in Iran and Denmark, the other primarily in Norway. There were also varying degrees of admixture in England, Sweden, Finland and Latvia. Approximate Bayesian computation indicated two independent introductions of H. persicum from Iran to Europe: the first one in Denmark and the second one in England. Finland was subsequently colonized by English populations. In contrast to the contemporary hypothesis of English origin of Norwegian populations, we found Finland to be a more likely source for Norwegian populations, a scenario supported by higher estimated historical migration from Finland to Norway. Genetic diversity per se is not a primary determinant of invasiveness in H. persicum. Our results indicate that, due to either pre-adaptations or rapid local adaptations, introduced populations may have acquired invasiveness after subsequent introductions, once a suitable environment was encountered.

Glacial survival may matter after all: nunatak signatures in the rare European populations of two west-arctic species.

Biogeographers claimed for more than a century that arctic plants survived glaciations in ice-free refugia within the limits of the North European ice sheets. Molecular studies have, however, provided overwhelming support for postglacial immigration into northern Europe, even from the west across the Atlantic. For the first time we can here present molecular evidence strongly favouring in situ glacial persistence of two species, the rare arctic-alpine pioneer species Sagina caespitosa and Arenaria humifusa. Both belong to the 'west-arctic element' of amphi-Atlantic disjuncts, having their few and only European occurrences well within the limits of the last glaciation. Sequencing of non-coding regions of chloroplast DNA revealed only limited variation. However, two very distinct and partly diverse genetic groups, one East and one West Atlantic, were detected in each species based on amplified fragment length polymorphisms (AFLPs), excluding postglacial dispersal from North America as explanation for their European occurrences. Patterns of genetic diversity and distinctiveness indicate that glacial populations existed in East Greenland and/or Svalbard (A. humifusa) and in southern Scandinavia (S. caespitosa). Despite their presumed lack of long-distance dispersal adaptations, intermixed populations in several regions indicate postglacial contact zones. Both species are declining in Nordic countries, probably due to climate change-induced habitat loss. Little or no current connectivity between their highly fragmented and partly distinct populations call for conservation of several populations in each geographic region.