The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution

Abstract

The earliest evolution of the animals remains a taxing biological problem, as all extant clades are highly derived and the fossil record is not usually considered to be helpful. The rise of the bilaterian animals recorded in the fossil record, commonly known as the 'Cambrian explosion', is one of the most significant moments in evolutionary history, and was an event that transformed first marine and then terrestrial environments. We review the phylogeny of early animals and other opisthokonts, and the affinities of the earliest large complex fossils, the so-called 'Ediacaran' taxa. We conclude, based on a variety of lines of evidence, that their affinities most likely lie in various stem groups to large metazoan groupings; a new grouping, the Apoikozoa, is erected to encompass Metazoa and Choanoflagellata. The earliest reasonable fossil evidence for total-group bilaterians comes from undisputed complex trace fossils that are younger than about 560 Ma, and these diversify greatly as the Ediacaran-Cambrian boundary is crossed a few million years later. It is generally considered that as the bilaterians diversified after this time, their burrowing behaviour destroyed the cyanobacterial mat-dominated substrates that the enigmatic Ediacaran taxa were associated with, the so-called 'Cambrian substrate revolution', leading to the loss of almost all Ediacara-aspect diversity in the Cambrian. Why, though, did the energetically expensive and functionally complex burrowing mode of life so typical of later bilaterians arise? Here we propose a much more positive relationship between late-Ediacaran ecologies and the rise of the bilaterians, with the largely static Ediacaran taxa acting as points of concentration of organic matter both above and below the sediment surface. The breaking of the uniformity of organic carbon availability would have signalled a decisive shift away from the essentially static and monotonous earlier Ediacaran world into the dynamic and burrowing world of the Cambrian. The Ediacaran biota thus played an enabling role in bilaterian evolution similar to that proposed for the Savannah environment for human evolution and bipedality. Rather than being obliterated by the rise of the bilaterians, the subtle remnants of Ediacara-style taxa within the Cambrian suggest that they remained significant components of Phanerozoic communities, even though at some point their enabling role for bilaterian evolution was presumably taken over by bilaterians or other metazoans. Bilaterian evolution was thus an essentially benthic event that only later impacted the planktonic environment and the style of organic export to the sea floor.

Ediacaran developmental biology

“…Grazhdankin et al ., 2008). It has been variously compared to algae (Ford, 1958), fungi (Peterson, Waggoner, & Hagadorn, 2003), stem‐metazoans (Budd & Jensen, 2017), pennatulacean cnidarians (Glaessner, 1984), or placed in a hypothetical non‐metazoan higher order group (Seilacher, 1989, 1992). Known Charnia masoni specimens range from ∼1 cm (Liu et al ., 2012) to >65 cm (Boynton & Ford, 1995) in length, with size variants typically interpreted as different ontogenetic stages in the Charnia life cycle (e.g.…”

“…Members of Erniettomorpha have been considered to show morphological similarities to members of the annulated Dickinsonia ‐like taxa (e.g. Budd & Jensen, 2017), but whether this evidences a phylogenetic relationship is unclear. The relative consistency of overall form in erniettomorphs suggests that they do not exhibit parallel modular growth and, thus, they are unlikely to be plants or algae.…”

“…The asymmetric head region of Yorgia has been speculatively likened to two of the three branch‐like structures that make up Tribrachidium (Budd & Jensen, 2017), implying axial homology between the dorso‐ventral axis of Tribachidium and the ‘anteroposterior’ axis of dickinsoniomorphs. In the absence of an asymmetric undivided region in some dickinsoniomorphs, and even in some Dickinsonia specimens, we do not consider that there are sufficient grounds to consider these axes to be homologous.…”

“…Many of these organisms, which are typically preserved only as impressions of their external surfaces, are united by a body plan composed of self‐repeating morphological units. Their fossil remains possess few morphological characters that are diagnostic of any particular phylogenetic affinity, and multiple competing hypotheses for where they lie within Eukarya have been proposed since their initial description (summarised in Xiao & Laflamme, 2009; Budd & Jensen, 2017), including the suggestion that they represent an entirely distinct Kingdom Vendobionta (Seilacher, 1989, 1992). This latter hypothesis later softened to consider the Ediacaran Biota as an extinct phylum within total‐group Metazoa or total‐group Eumetazoa (Buss & Seilacher, 1994); a view not substantially different from the current broad consensus that these Ediacaran organisms are allied to early‐branching lineages of Metazoa or Eumetazoa (e.g.…”

“…This latter hypothesis later softened to consider the Ediacaran Biota as an extinct phylum within total‐group Metazoa or total‐group Eumetazoa (Buss & Seilacher, 1994); a view not substantially different from the current broad consensus that these Ediacaran organisms are allied to early‐branching lineages of Metazoa or Eumetazoa (e.g. Xiao & Laflamme, 2009; Budd & Jensen, 2017). Surprisingly, in many cases this consensus does not rest on material evidence of metazoan affinity but, rather, on an implicit assumption that the organisms are total‐group metazoans.…”