Biol Rev Camb Philos Soc. 2025 Nov 9. doi: 10.1111/brv.70101. Online ahead of print.
ABSTRACT
The first eukaryotes evolved from their archaean ancestors in the early Proterozoic, likely ca. 2000-1800 million years ago (Mya). Their macroscopic multicellular descendants, such as plants, heterokont algae, animals and fungi, appeared hundreds of million years later. During this intermediate period of eukaryote evolution, dozens of important protist lineages emerged, either unicellular or with only simple forms of multicellularity. Recent discoveries and phylogenetic analyses point to the branching order at the base of the eukaryote family tree and suggest a sequence of evolutionary and ecological events that likely took place during the Palaeoproterozoic. I review the 25 ‘small lineages’ of protists, such as malawimonads, trimastigids, barthelonids, ancyromonads, breviatids, provorans, telonemids, aquavolonids and colponemids, that typically fall outside major eukaryote clades (such as opisthokonts, archaeplastidians, dinophytes, ciliates, or apicomplexans). For each such lineage, general features of anatomy, trophic mode, ecology and behaviour are assembled from published literature. Three characters were determined for all 25 lineages and their 21 ‘outgroups’, and are reported as a character state matrix: (i) oxygen preferences (anaerobic, microaerobic, aerobic); (ii) trophic mode (autotrophic, mixotrophic, symbiotrophic, phagotrophic, osmotrophic, myzocytotic); and (iii) motility (immobile, swimming, gliding, amoeboid). This summary of basic lifestyle information for all 46 eukaryotic lineages allows a tentative ancestral state reconstruction for all major eukaryotic clades (including the supergroups Opisthokonta, Amoebozoa, Archaeplastida, Rhizaria, Alveolata and Stramenopiles), and the whole clade Eukaryota. The summary is also presented in the form of an evolutionary-ecological hypothesis for early eukaryote evolution in four stages. In Stage I, the ancestral eukaryote was an ‘excavate-like’ biflagellate bacterivore with a ventral depression, most likely microaerophilic. In Stage II, the first major evolutionary innovation occurred: adaptation to life at the sediment surface by a podiate-like protist that was capable of gliding mobility and pseudopodial formation. ‘Sulcozoan’ amoeboflagellates (mantamonads, breviatids, apusomonads, etc.) represent this grade of organisation. In Stage III, the common ancestor of Provora and Telonemia+Rhizaria+Alveolata+Stramenopiles (TSAR) evolved the capability to feed on bacteria and some eukaryotes (facultative eukaryovory), which was made possible by increased fidelity of swimming (i.e. quick turning via rapid change of flagellar beat pattern) and cytoskeletal innovations. In Stage IV more specialised predators emerged: obligatory eukaryovores (probably colponemid-like) with specialized feeding apparatuses and amoebozoans that evolved from sulcozoan ancestors by growth of cell size and other features that allowed them to invade bacterial films. A suite of adaptations to the emergence of predators followed throughout the eukaryote family tree.
PMID:41208008 | DOI:10.1111/brv.70101
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