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

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.

The Weng'an Biota (Doushantuo Formation): an Ediacaran window on soft-bodied and multicellular microorganisms

“…The age of the biota has been debated (Budd 2008;Erwin & Valentine 2013;Xiao et al 2014a;Yin et al 2015), with arguments focusing on the correlation of two karstic surfaces, one at the top of Unit 3 and the other within Unit 5 (for detailed discussion of Doushantuo correlation see Zhu et al (2007), Zhu et al (2013) and Yang et al (2015)). If the lower surface is correlated to the c. 582 Ma Gaskiers glaciation (Condon et al 2005) then the biota would be younger than 582 Ma.…”

“…If the lower surface is correlated to the c. 582 Ma Gaskiers glaciation (Condon et al 2005) then the biota would be younger than 582 Ma. However, the lower surface may be older (Yin et al 2015) and, if the upper karstic surface correlates to the Gaskiers glaciation (Xiao et al 2014a), then the biota would be older than 582 Ma. Direct radiometric dates for Unit 4 at Weng'an have been inconclusive, giving Pb-Pb isochron ages of 572 ± 36 Ma for Unit 4A (Y.…”

“…Some simpler forms, such as Archaeophycus (Fig. 2j), show interesting similarities to extant bangialean red algae (Xiao et al 1998), although other affinities cannot be ruled out (Xiao et al 2014a). More complex forms such as Thallophyca and Paramecia share characters with floridophyte red algae including pseudoparenchymous construction, differentiated thalli and possible reproductive structures .…”

“…However, subsequent analyses have cast doubt on this view, and there is currently much disagreement over these interpretations (Bailey et al 2007a;Huldtgren et al 2011;Bengtson et al 2012;L. Chen et al 2014, Xiao et al 2014a. Here, we review the stratigraphic position, geological age and environmental setting of the deposit, and present an overview of the biota and an assessment of the phylogenetic affinities of the various taxa.…”

Carbonaceous biosignatures of diverse chemotrophic microbial communities from chert nodules of the Ediacaran Doushantuo Formation

“…The Ediacaran Doushantuo Formation (DST) of South China preserves an exceptional geological record to help decode the co-evolution of life and the Earth system during the ProterozoicPhanerozoic transition (Xiao et al, 2014a). Highly diverse fossils have been reported in the DST, including possible metazoan embryos (Xiao et al, 1998Chen et al, 2004Chen et al, , 2009Hagadorn et al, 2006;Yin et al, 2007), cyanobacteria, sulfur bacteria, multicellular algae, and acanthomorphic acritarchs (Xiao, 2004;Xiao et al, 2014b;McFadden et al, 2008McFadden et al, , 2009Bailey et al, 2013).…”