Age of Neoproterozoic Bilatarian Body and Trace Fossils, White Sea, Russia: Implications for Metazoan Evolution

Martin, Mark W.; Гражданкин, Д. В.; Bowring, Samuel A.; Evans, David A.D.; Fedonkin, M. A.; Kirschvink, Joseph L.

doi:10.1126/science.288.5467.841

Cited by 343 publications

(107 citation statements)

References 26 publications

(31 reference statements)

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“…The ME estimate of 634-604 Ma for the origin of eumetazoan characters places it in the early part of the newly established Ediacaran period (27) (31)]. Interestingly, it is also when animals make their first appearance in the fossil record, first as taxonomically unresolved embryos in rocks from the mid-upper Doushantuo Formation (Fm) of South China (32), inferred to be no younger than Ϸ580 Ma (30), followed by unambiguously eumetazoan trace fossils in the Ͼ558-Ma Verkhovka Fm of Northwest Russia (33,34). Neither of these data points, however, can be used as an even approximate measure of first appearance, due to their dependence on exceptional preservation and͞or macroscopic size (35).…”

Section: Resultsmentioning

confidence: 99%

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

Peterson

Butterfield

2005

Proc. Natl. Acad. Sci. U.S.A.

322

219

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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...

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Section: Resultsmentioning

confidence: 99%

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

Peterson

Butterfield

2005

Proc. Natl. Acad. Sci. U.S.A.

322

219

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“…40). The bilaterian trace fossil record would commence only after the invention of pattern formation mechanisms that potentiated the evolution of larger body size in multiple animal clades near the end of Neoproterozoic (41,42). Whether the origin of bilaterians or any other metazoan group can be triggered by environmental perturbations such as ''snowball Earth'' (43,44) remains highly speculative at the moment, given the uncertainty about the exact number and ages of Neoproterozoic glaciations (45).…”

Section: Tempo and Mode Of Early Animal Evolutionmentioning

confidence: 99%

Estimating metazoan divergence times with a molecular clock

Peterson

Lyons

Nowak

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

400

285

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Accurately dating when the first bilaterally symmetrical animals arose is crucial to our understanding of early animal evolution. The earliest unequivocally bilaterian fossils are Ϸ555 million years old. In contrast, molecular-clock analyses calibrated by using the fossil record of vertebrates estimate that vertebrates split from dipterans (Drosophila) Ϸ900 million years ago (Ma). Nonetheless, comparative genomic analyses suggest that a significant rate difference exists between vertebrates and dipterans, because the percentage difference between the genomes of mosquito and fly is greater than between fish and mouse, even though the vertebrate divergence is almost twice that of the dipteran. Here we show that the dipteran rate of molecular evolution is similar to other invertebrate taxa (echinoderms and bivalve molluscs) but not to vertebrates, which significantly decreased their rate of molecular evolution with respect to invertebrates. Using a data set consisting of the concatenation of seven different amino acid sequences from 23 ingroup taxa (giving a total of 11 different invertebrate calibration points scattered throughout the bilaterian tree and across the Phanerozoic), we estimate that the last common ancestor of bilaterians arose somewhere between 573 and 656 Ma, depending on the value assigned to the parameter scaling molecular substitution rate heterogeneity. These results are in accord with the known fossil record and support the view that the Cambrian explosion reflects, in part, the diversification of bilaterian phyla.A lthough the Cambrian explosion is of singular importance to our understanding of the history of life, it continues to defy explanation (1). This defiance stems, in part, from our inability to distinguish between two competing hypotheses: whether the Cambrian explosion reflects the rapid appearance of fossils with animals having a deep but cryptic precambrian history, or whether it reflects the true sudden appearance and diversification of animals in the Cambrian (2). Because each hypothesis makes a specific prediction of when animals arose in time, one way to distinguish between these two hypotheses is to date animal diversifications by using a molecular clock (2). A number of previous clock studies (reviewed in refs. 3 and 4) have suggested that the last common ancestor of bilaterians (LCB) lived well over one billion years ago (5, 6), whereas others suggest that LCB arose Ϸ900 million years ago (Ma) (e.g., refs. 7-10), and still others are more consistent with an origination closer to the Cambrian (11-13). These deep estimates for the origin of LCB raise the question of how hundreds of millions of years of bilaterian evolution can escape detection, given that LCB and its near relatives should have had the capability of leaving both body and trace fossils (14-16).Because molecular clocks have several inherent problems, including how the clock is calibrated, how molecular substitution rates are estimated, and how heterogeneity in these rates is detected and corrected (3, 4), as well...

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“…Extant radially symmetrical animals are composed of two cell layers; an outer epithelium and a gastrodermis. Extant bilaterians are (5) Bemus (1988), (6) Bowring et al (2003a), (7) Bowring et al (2003b), (8) Compston et al (2002), (9) Martin et al (2000), (10) Grazhdankin (2004), (11) Preiss (2000) and (12) Grotzinger (1995). A solid line indicates that the date for a given formation or a member in the formation is relatively secure; while a dashed line indicates that the dating is not secure.…”

Section: Morphological Characterisation Of Ediacaran Generamentioning

confidence: 99%

“…There are two dates that constrain the age of the Verkhovka Formation; at the same time they define the top of the Lamtsa and the base of the Zimnegory Formations (Martin et al 2000;Grazhdankin 2004) at the White Sea sites. The date of 556 MA defines the base of the Rawnsley Quartzite in the Flinders Range (Preiss 2000); however, this date has a large standard deviation associated with it.…”

Section: Time Of First Appearance Of Ediacaran Genera and Their Geolomentioning

confidence: 99%

The rise of bilaterians

Freeman

2009

Historical Biology

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Recently Shen et al. have argued that the Ediacaran faunas from Avalon-Charnwood [580 -560 million years ago (MA)], the White Sea-Flinders Range (560-550 MA) and Namibia (550 -543 MA) occupied the same morphospace even though these faunas differed in species composition, ecology, biogeography and age. The traits they used to characterise these faunas could not distinguish between important promorphological features such as radial vs. bilaterian and unitary vs. colonial animals. Their inappropriate assignment of symmetry properties led to the homogenisation of morphospace in these different faunas. Another way to examine shifts in morphospace involves sorting out radial vs. bilaterian and unitary vs. colonial genera in terms of their time of first appearance in the fossil record. While genera with both kinds of symmetry properties and unitary and colonial animals were present during the early Ediacaran, there was a large proportional increase in new bilaterian genera and a decrease in colonial genera beginning between 560-550 MA. The increase in bilaterians may have been associated with the ability to exploit food sources in and on the substrate of shallow water environments.

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Age of Neoproterozoic Bilatarian Body and Trace Fossils, White Sea, Russia: Implications for Metazoan Evolution

Cited by 343 publications

References 26 publications

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

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

Estimating metazoan divergence times with a molecular clock

The rise of bilaterians

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