The Weng'an biota and the Ediacaran radiation of multicellular eukaryotes

Abstract

Abstract The rise of multicellularity represents a major evolutionary transition and it occurred independently in multiple eukaryote clades. Although simple multicellular organisms may have evolved in the Mesoproterozoic Era or even earlier, complex multicellular eukaryotes began to diversify only in the Ediacaran Period, just before the Cambrian explosion. Thus, the Ediacaran fossil record can provide key paleontological evidence about the early radiation of multicellular eukaryotes that ultimately culminated in the Cambrian explosion. The Ediacaran Weng'an biota in South China hosts exceptionally preserved eukaryote fossils, including various acanthomorphic acritarchs, pseudoparenchymatous thalli, tubular microfossils, and spheroidal fossils such as Megasphaera, Helicoforamina, Spiralicellula, and Caveasphaera. Many of these fossils have been interpreted as multicellular eukaryotes, although alternative interpretations have also been proposed. In this review, we critically examine these various interpretations, focusing particularly on Megasphaera, which has been variously interpreted as a sulfur-oxidizing bacterium, a unicellular protist, a mesomycetozoean-like holozoan, a volvocine green alga, a stem-group animal, or a crown-group animal. We conclude that Megasphaera is a multicellular eukaryote with evidence for cell-to-cell adhesion, a flexible membrane unconstrained by a rigid cell wall, spatial cellular differentiation, germ–soma separation, and programmed cell death. These features are inconsistent with the bacterium, unicellular protist, and mesomycetozoean-like holozoan interpretations. Thus, the surviving hypotheses, particularly the stem-group animal and algal interpretations, should be further tested with additional evidence. The Weng'an biota also hosts cellularly differentiated pseudoparenchymatous thalli with specialized reproductive structures indicative of an affinity with florideophyte red algae. The other Weng'an fossils reviewed here may also be multicellular eukaryotes, although direct cellular evidence is lacking in some and phylogenetic affinities are poorly constrained in others. The Weng'an biota offers many research opportunities to resolve the life histories and phylogenetic diversity of early multicellular eukaryotes and to illuminate the evolutionary prelude to the Cambrian explosion.