The Early Ediacaran Caveasphaera Foreshadows the Evolutionary Origin of Animal-like Embryology

Abstract

The Ediacaran Weng'an Biota (Doushantuo Formation, 609 million years old) is a rich microfossil assemblage that preserves biological structure to a subcellular level of fidelity and encompasses a range of developmental stages [1]. However, the animal embryo interpretation of the main components of the biota has been the subject of controversy [2, 3]. Here we describe the development of Caveasphaera, which varies in morphology from lensoid, to a hollow spheroidal cage [4], to a solid spheroid [5], but has largely evaded description and interpretation. Caveasphaera is demonstrably cellular and develops within an envelope by cell division and migration, first defining the spheroidal perimeter via anastomosing cell masses that thicken and ingress as strands of cells that detach and subsequently aggregate in the polar region. Concomitantly, the overall diameter increases as does the volume of the cell mass but, after an initial phase of reductive palinotomy, the volume of individual cells remains the same through development. The process of cell ingression, detachment and polar aggregation is analogous to gastrulation; together with evidence of functional cell adhesion and development within an envelope, this is suggestive of a holozoan affinity. Maternal investment in the embryonic development of Caveasphaera and co-occuring Tianzhushania and Spiralicellula, as well as delayed onset of later development, may reflect an adaptation to the heterogeneous nature of the early Ediacaran nearshore marine environments in which early animals evolved. RESULTS The Weng'an biota provides a unique insight into multicellular life in the early Ediacaran period during which molecular clocks estimate the fundamental animal lineages to have diverged [6]. Indeed, there are numerous claims of animal remains from the biota, including miniature adult eumetazoans [7] and bilaterians [8], and embryonic animals [2, 9-12], but all remain contentious [3, 13-18]. However, there is a broader diversity of fossil remains from this deposit that have been the subject of little attention, some of which may have a greater claim on animal affinity. These fossils include Caveasphaera costata (Figure 1) which has been described as a spherical hollow cage (Figure 1A-C) [4] to a more solid sphere (Figure 1D) [5] of unknown nature and affinity, though superficial comparison has been drawn to embryos of an octocoral [4]. Analysis of the structure and development of Caveasphaera is challenging because of its small size and complex morphology. We employed Synchrotron Radiation X-ray Tomographic Microscopy (srXTM) [19] and High resolution Xray microtomography [20] to analyse 233 specimens of Caveasphaera that encompass its morphological and size range, based on a rich fossil assemblage from '54' and Datang quarries in the

Survival and selection biases in early animal evolution and a source of systematic overestimation in molecular clocks

“…It is true that there are no traces of crown-group metazoans in the Bitter Springs and Svanbergfjellet Formation biotas; but the same is surely also true of both the Lantian and the Weng'an biota. The latter in particular preserves a series of intriguing and much debated embryo-like balls of cells, but despite this demonstrating the possibility of crown group metazoans being preserved here [109], none have to date been found that have commanded anything close to universal assent [110]. Furthermore, although [108] regard the Lantian as providing the soft maximum for bilaterians, there is (also) surely no evidence for them in the Weng'an biota either (or, indeed, the Avalonian 'Ediacaran' assemblages).…”

The origin of animal body plans: a view from fossil evidence and the regulatory genome

“…Initially described as animal embryos (Xiao and Knoll, 2000), the affinities of these fossils have been linked to various protists, sulfur-oxidizing bacteria, volvocine green algae and embryonic, larval or adult animals (reviewed by Xiao et al, 2014;Cunningham et al, 2017b). One form, Caveasphaera, exhibits patterns of cellular development analogous to gastrulation in animals, and has been plausibly assigned a holozoan, but not necessarily metazoan, affinity (Yin et al, 2019) (Node 1, Fig. 1).…”

Developmental biology of Helicoforamina reveals holozoan affinity, cryptic diversity, and adaptation to heterogeneous environments in the early Ediacaran Weng’an biota (Doushantuo Formation, South China)

“…In the history of interpretations of the Weng'an biota, Y-shaped cell interfaces are seen also in Megasphaera, where they have been commonly interpreted to indicate animal affinity (5,12,22); however, Y-shaped cell interfaces are encountered in embryo-like conformations of cells in diverse eukaryotes including ciliates, rhodophytes, and nonmetazoan holozoans (18). Yin et al (13) reviewed the diversity of embryo-like developmental stages that occur in eukaryotes. Among these, the known developmental stages of Helicoforamina bear a strong resemblance to the early binary reductive palintomic stages of rhodophyte embryos (23,24).…”