Abstract
Sedimentary ancient DNA has been proposed as a key methodology for reconstructing biodiversity over time. Yet, despite the concentration of Earth’s biodiversity in the tropics, this method has rarely been applied in this region. Moreover, the taphonomy of sedimentary DNA, especially in tropical environments, is poorly understood. This study elucidates challenges and opportunities of sedimentary ancient DNA approaches for reconstructing tropical biodiversity. We present shotgun-sequenced metagenomic profiles and DNA degradation patterns from multiple sediment cores from Mubwindi Swamp, located in Bwindi Impenetrable Forest (Uganda), one of the most diverse forests in Africa. We describe the taxonomic composition of the sediments covering the past 2200 years and compare the sedimentary DNA data with a comprehensive set of environmental and sedimentological parameters to unravel the conditions of DNA degradation. Consistent with the preservation of authentic ancient DNA in tropical swamp sediments, DNA concentration and mean fragment length declined exponentially with age and depth, while terminal deamination increased with age. DNA preservation patterns cannot be explained by any environmental parameter alone, but age seems to be the primary driver of DNA degradation in the swamp. Besides degradation, the presence of living microbial communities in the sediment also affects DNA quantity. Critically, 92.3% of our metagenomic data of a total 81.8 million unique, merged reads cannot be taxonomically identified due to the absence of genomic references in public databases. Of the remaining 7.7%, most of the data (93.0%) derive from Bacteria and Archaea, whereas only 0-5.8% are from Metazoa and 0-6.9% from Viridiplantae, in part due to unbalanced taxa representation in the reference data. The plant DNA record at ordinal level agrees well with local pollen data but resolves less diversity. Our animal DNA record reveals the presence of 41 native taxa (16 orders) including Afrotheria, Carnivora, and Ruminantia at Bwindi during the past 2200 years. Overall, we observe no decline in taxonomic richness with increasing age suggesting that several-thousand-year-old information on past biodiversity can be retrieved from tropical sediments. However, comprehensive genomic surveys of tropical biota need prioritization for sedimentary DNA to be a viable methodology for future tropical biodiversity studies.
Highlights
The tropics hold the greatest biodiversity on Earth (e.g., Gaston, 2000; Jenkins et al, 2013) containing about three quarters of all species (Barlow et al, 2018)
Our study highlights challenges and opportunities of Sedimentary ancient DNA (sedaDNA) approaches for reconstructing tropical biodiversity which we identify from the investigation of multiple profiles from a tropical swamp located within an exceptionally diverse African rainforest
We present one of the richest biogeological and DNA datasets for tropical sediments yet published
Summary
The tropics hold the greatest biodiversity on Earth (e.g., Gaston, 2000; Jenkins et al, 2013) containing about three quarters of all species (Barlow et al, 2018). In particular tropical rainforests – the most diverse terrestrial ecosystems – are largely characterized by a poor fossil record (Wing et al, 2009; Jacobs et al, 2010), which severely limits the reconstruction of diversity patterns. The mammalian fossil record for the past 20,000 years of Africa only contains few taxa from the large Congo Basin (Jousse, 2017) where several hundreds of mammal species occur today (Jenkins et al, 2013). Floristic diversity can be reconstructed from pollen records, but generally suffer from limited taxonomic resolution in comparison to the existing tropical plant diversity (e.g., Morley, 2000). A comprehensive picture of the history of tropical biodiversity is still far from being established
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