A critical reappraisal of the fossil record of the bilaterian phyla

Abstract

It has long been assumed that the extant bilaterian phyla generally have their origin in the Cambrian explosion, when they appear in an essentially modern form. Both these assumptions are questionable. A strict application of stem- and crown-group concepts to phyla shows that although the branching points of many clades may have occurred in the Early Cambrian or before, the appearance of the modern body plans was in most cases later: very few bilaterian phyla sensu stricto have demonstrable representatives in the earliest Cambrian. Given that the early branching points of major clades is an inevitable result of the geometry of clade diversification, the alleged phenomenon of phyla appearing early and remaining morphologically static is seen not to require particular explanation. Confusion in the definition of a phylum has thus led to attempts to explain (especially from a developmental perspective) a feature that is partly inevitable, partly illusory. We critically discuss models for Proterozoic diversification based on small body size, limited developmental capacity and poor preservation and cryptic habits, and show that the prospect of lineage diversification occurring early in the Proterozoic can be seen to be unlikely on grounds of both parsimony and functional morphology. Indeed, the combination of the body and trace fossil record demonstrates a progressive diversification through the end of the Proterozoic well into the Cambrian and beyond, a picture consistent with body plans being assembled during this time. Body-plan characters are likely to have been acquired monophyletically in the history of the bilaterians, and a model explaining the diversity in just one of them, the coelom, is presented. This analysis points to the requirement for a careful application of systematic methodology before explanations are sought for alleged patterns of constraint and flexibility.

Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil

“…The Corumbá Group trace fossils place an important latest Ediacaran (541-555 Ma) minimum constraint on the origin of meiofaunal animals and their interactions with soft substrates. Meiofauna are ubiquitous in both modern marine and freshwater environments, and their origin in deep time has been often discussed 21,22 but little explored from an evidential palaeontological perspective. Extant meioendobenthic organisms are particularly important contributors to biogeochemical cycling, microbial ecology and ecosystem productivity, especially in muddy sediments 27,37 .…”

“…Assuming that contemporary molecular clock analyses yield accurate, if imprecise 18 , node ages for animal divergences, a small body size and concomitant limited fossilization potential 21 could reconcile these discordant records of animal evolution (but see ref. 22 ).The small body size of the ancestral bilaterian is supported by recent phylogenomic analyses of deep animal relationships, with acoel flatworms and xenoturbellids (Xenacoelomorpha) being a sister group to all remaining bilaterians (Nephrozoa) 23 , and smallbodied spiralian taxa (the 'Platyzoa') recognized as a paraphyletic grade with respect to macroscopic trochozoans 24 . This suggests that early bilaterians and spiralians were small bodied, possibly meiofaunal, and moved using ciliary gliding.…”

“…Assuming that contemporary molecular clock analyses yield accurate, if imprecise 18 , node ages for animal divergences, a small body size and concomitant limited fossilization potential 21 could reconcile these discordant records of animal evolution (but see ref. 22 ).…”

Origins of the other metazoan body plans: the evolution of larval forms

“…These ancestral bilaterians were direct developers and had evolved the basic developmental gene regulatory systems of bilaterian development. With the opening of the Cambrian radiation, the evolution of more divergent bilaterians accelerated and produced the basal clades that gave rise to modern phyla and their precursors (Budd & Jensen 2000), but planktonic larvae and their body plans evolved secondarily. The requirements for a planktonic larva are simpler than for the larger benthic reproductive adult.…”

Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

“…This debate has mostly revolved around two different datasets: the bodyfossil record and molecular clocks. Although the body-fossil record supports the notion that the Cambrian event of diversification is real and unparalleled in the history of life [9,10], interpretation of molecular clock evidence has been quite controversial. Earlier studies did not support the explosion scenario, suggesting deeper divergence among animals [11,12].…”