Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record

Abstract

Molecular clocks have the potential to shed light on the timing of early metazoan divergences, but differing algorithms and calibration points yield conspicuously discordant results. We argue here that competing molecular clock hypotheses should be testable in the fossil record, on the principle that fundamentally new grades of animal organization will have ecosystem-wide impacts. Using a set of seven nuclear-encoded protein sequences, we demonstrate the paraphyly of Porifera and calculate sponge͞eumetazoan and cnidarian͞bilaterian divergence times by using both distance [minimum evolution (ME)] and maximum likelihood (ML) molecular clocks; ME brackets the appearance of Eumetazoa between 634 and 604 Ma, whereas ML suggests it was between 867 and 748 Ma. Significantly, the ME, but not the ML, estimate is coincident with a major regime change in the Proterozoic acritarch record, including: (i) disappearance of low-diversity, evolutionarily static, pre-Ediacaran acanthomorphs; (ii) radiation of the high-diversity, short-lived Doushantuo-Pertatataka microbiota; and (iii) an orderof-magnitude increase in evolutionary turnover rate. We interpret this turnover as a consequence of the novel ecological challenges accompanying the evolution of the eumetazoan nervous system and gut. Thus, the more readily preserved microfossil record provides positive evidence for the absence of pre-Ediacaran eumetazoans and strongly supports the veracity, and therefore more general application, of the ME molecular clock.Porifera ͉ acritarchs ͉ Ediacaran ͉ coevolution T he sudden appearance of diverse metazoan fossils Ϸ530 million years ago (Ma) is the focus of ongoing and heated debate: Is this recording a true ''Cambrian explosion'' of early metazoan evolution or merely the onset of extensive burrowing and biomineralization (1)? Certainly the invisibility of microscopic, nonburrowing, and͞or nonbiomineralizing metazoans in the fossil record allows for the possibility of deep Proterozoic origins, so independent lines of evidence must be sought. Molecular clocks offer a potentially powerful approach for testing such evolutionary hypotheses (2), but recent analyses have yielded conspicuously discordant results. Pisani et al. (3), for example, estimate that the protostome-deuterostome ancestor evolved 900-1,100 Ma, whereas Douzery et al. (4) place this node at 642-761 Ma and Peterson et al. (5) at Ϸ570 Ma. With estimated divergence times differing by Ͼ500 million years (myr), there is clearly a need to assess both the methods used and predictions made by individual molecular-clocks analyses.Pisani et al. (3) have argued that their deep estimate for metazoan origins is robust because it agrees with a previous analysis calibrated by using different taxa, i.e., between chick and mouse (6) vs. centipedes and millipedes and spiders and horseshoe crabs (3). However, Peterson et al. (5) demonstrated that a significant rate reduction is associated with the vertebrate sequences, such that a vertebrate-calibrated clock produces a spurious 2-fold ove...

The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans

“…Choanoflagellates, sponges and other metazoans last shared a unicellular common ancestor in the late Precambrian period, more than 600 million years ago 41,42 . Although the origin of metazoans was a pivotal event in life's history, little is known about the genetic underpinnings of the requisite transition to multicellularity.…”

Darwin's dilemma: the realities of the Cambrian ‘explosion’

“…It remains the case, however, that the functional link between fluid flow around acritarchs and capture remains to be explored, as does the discovery of faecal pellets containing such acritarchs. Peterson & Butterfield (2005) estimates of metazoan diversification still significantly predate the bulk of the Ediacaran record, which as noted below has many problematic aspects. To date the links between these assemblages and the proposed synthesis of Peterson & Butterfield (2005) are somewhat tenuous.…”

“…Peterson & Butterfield (2005) estimates of metazoan diversification still significantly predate the bulk of the Ediacaran record, which as noted below has many problematic aspects. To date the links between these assemblages and the proposed synthesis of Peterson & Butterfield (2005) are somewhat tenuous. Nor is the typical Ediacaran taphonomy particularly conducive to preserving the delicate grazers and other metazoans that are posited to have existed.…”

“…Nevertheless, it still exists. Peterson & Butterfield (2005), for example, offer an interesting synthesis that ties together geological, molecular and palaeontological data. Yet their analysis begs several questions.…”

Neoproterozoic microfossils from the margin of the East European Platform and the search for a biostratigraphic model of lower Ediacaran rocks

“…Post-Sturtian but pre-Marinoan biology remains poorly documented, so it is hard to know whether inferred extinctions accompanied Sturtian or Marinoan glaciation. Available data also suggest that the major biological reorganization represented by ECAP microfossils occurred well after Marinoan deglaciation, in association with mid-Ediacaran redox change (Fike et al, 2006;Canfield et al, 2007;McFadden et al, 2008), animal radiation (Peterson and Butterfield, 2005;Yin et al, 2007), or the Acraman impact event (Grey et al, 2003). To the extent that at least some ECAP fossils preserve egg or diapause cysts of early metazoans (Yin et al, 2007), the ECAP radiation may signal the expansion of animals with resting stages in their life cycles (Marcus and Boero, 1998).…”