Ancient environmental DNA reveals shifts in dominant mutualisms during the late Quaternary

Using ancient DNA, it is possible to study the species and communities that inhabited past landscapes. However, finding more or less intact ancient DNA is challenging because DNA degrades quickly. One possible source of intact ancient DNA is permafrost. The paleoecological research team, led by professor Eske Willerslev from the University of Copenhagen, in collaboration with EU project (GOCE-2006-036866) and an international network of researchers, generated an extensive environmental DNA (eDNA) dataset describing past vegetation at sites across the northern high latitudes (Siberia, Alaska and Yukon) during the last 50,000 years. The resulting DNA-based ‘snapshots’ of ancient vegetation showed (see Willerslev et al. 2014) that the composition of high-latitude plant communities has changed considerably during the late Quaternary. Surprisingly, the plant communities that existed prior to the Last Glacial Maximum (pre-LGM, 50-25kY BP) were more diverse, and contained more forbs, than those emerging during (LGM, 25-15ky BP) or since the LGM (post-LGM, <15ky BP).

Although Willerslev et al.’s 2014 paper provided a description of ancient vegetation and linked it with information about megaherbivore diet and occurrence, parallel changes in positive (i.e., mutualistic) interactions involving past vegetation remained unexplored. Nonetheless, recent studies of contemporary plant communities have shown that mutualistic relationships play crucial roles in shaping plant community structure and function.

Here we show how mutualisms involving plants and several heterotrophic organisms (including fungi, bacteria and insects) varied during the last 50,000 years. During the preLGM – a fluctuating but generally cool period – arbuscular mycorrhizal (AM) and non-N-fixing plants predominated. During the LGM – a cold, arid period – the representation of ectomycorrhizal (ECM), non-mycorrhizal (NM) and facultatively mycorrhizal plants increased, while that of N-fixing plants decreased further. During the post-LGM – marking the transition to and establishment of the current Holocene interglaciation – representation of AM plants decreased further, while that of ECM, NM, N-fixing and wind-pollinated plants increased.

These changes to the mutualist trait structure of vegetation through the cooler and warmer periods of the late Quaternary do not generally reflect contemporary relationships observed in relation to latitude Rather, they may reflect responses to historical environmental conditions that are without current analogue. For instance, compared with earlier periods, the post-LGM period can be characterized by higher precipitation, atmospheric CO₂ and nitrogen limitation. Our results are in line with several recent experiments showing that under higher temperature and CO2, ECM gain dominance over AM plant species, because they cope better with increasing nitrogen shortage. However, the study period also witnessed the extinction of many megaherbivores, as well the first major human impacts on ecosystems, and such biotic factors may also have influenced the mutualist trait structure of plant communities. Furthermore, mutualistic partnerships may have been influenced by biogeographic processes such as spatial decoupling of partners – certain partners may have reached deglaciated areas more effectively than others.

Many forecasts of the impact of climate change on biodiversity are made using macroecological or species distribution models that incorporate information about current relationships between organisms and climate parameters, often temperature. The results of the current study show, however, that the patterns of mutualist trait abundance seen along contemporary latitudinal gradients do not necessarily make good predictors of variations in trait abundance during periods of climate change.