Renewing the utility of fossil evidence for the rise of eukaryotes

Eukaryotes (complex organisms whose cells have membrane-bound organelles) have evolved to dominate the modern biosphere1, 2 . Their diversification during the Neoproterozoic Era (1,000-539 million years ago, Ma) had profound consequences for our planet and its biology3, 4; eukaryotes replaced cyanobacteria as the dominant primary producers5, 6 and emerged as prominent ecosystem engineers that modulated biogeochemical cycles and altered predator-prey dynamics . Despite the central importance of eukaryotes to the foundation of the modern biosphere, much remains unknown about the triggers, tempo, and ecology of their initial evolutionary radiation.

The principal challenge has been the paucity of early fossils that can be placed accurately in phylogenies and are preserved in well-dated geological successions . The earliest eukaryotes were microscopic with delicate sub-cellular features and lacked mineralised hard parts10, 11; consequently, we are reliant on instances of exceptional preservation to document their evolution . Of the documented fossils that are older than 600 Ma, only three can be confidently allied to modern eukaryote groups: the red alga Bangiomorpha , the green alga Proterocladus , and testate amoebae represented by vase-shaped microfossils.

The rarity of such fossils has encouraged the use of complementary approaches to reconstruct the early history of eukaryotes. Molecular clocks, which use the genetic data encoded in modern eukaryotes, predict the diversification of major eukaryotic groups (e.g., red algae) by~1,000 Ma. However, these predictions generally have large uncertainties spanning hundreds of millions of years. Ancient chemical biomarkers provide a more direct method of reconstructing the history of early eukaryotes. The presence of protosteroids in sedimentary rocks ~1,600 Ma is consistent with a late Palaeoproterozoic origin of eukaryotes, while ~800 Macholesteroids and ~635 Ma stigmasteroids document the rise of crown eukaryotes through the Neoproterozoic5, 23 (Fig. 1). However, concerns over modern contamination and the impact of taphonomic bias , as well as an inadequate understanding of how biomarkers map to phylogeny, challenge their utility.

The issues with these complementary lines of evidence highlight the importance of the Proterozoic microfossil record: it provides the only direct evidence of early eukaryotes and their ecologies.

Aims/Methods
My DPhil will address two of the major shortcomings of using the fossil record to reconstruct early eukaryote evolution: (i) the rarity of fossils with enough morphological characters to be assigned to modern groups and (ii) an inability to precisely identify what organisms these fossils represent.