This section focuses on a debate (https://youtu.be/XrHrjTDn-tY ) between leading paleontologists about the time of origin of the vertebrates and the rest of the animal kingdom. The debate focuses on the difference between the fossil record and molecular clock estimates. Subjects include molecular clocks (Phillip Donoghue), Cambrian and Precambrian paleontology (Alison Daly), genetics (Peter Holland), and Precambrian microorganisms and geochemistry (Rosalind Rickaby). This section begins with background on molecular clock studies of vertebrates and early animal evolution.
Most paleontologists think that the animal kingdom began with the Ediacaran biota in the Avalon Explosion. Bilaterian animals do not appear prior to the Cambrian in 541 Ma; thus, divergence of protostomes and deuterostomes took place after the beginning of the Cambrian; however, molecular clocks indicate that the divergence between protostomes and deuterostomes took place before the Avalon Explosion.
Molecular clocks predict divergence times between species based on the difference in genes in the two species and the known rates of DNA change. Not all genes mutate at predictable rates; however, the types of genes used in molecular clocks mutate at predictable rates. Vertebrates have a slow mutation rate of these particular genes. The mutation rate is based on rates of mutation, copying errors, radiation, and other factors. Scientists can predict the rate of change by examining the time that organisms diverged in the fossil record and comparing this to the number of changes in the genome that happened since the divergence. In general, researchers can use known rates of DNA mutation, and simply look at the differences in known genomes of existing phyla in order to estimate the time that groups of animals diverged. Molecular clocks are constrained by the fossil record, but there are no vertebrates in the fossil record prior to the Early to Middle Cambrian so it is challenging to estimate the early part of the molecular clock for vertebrates.
In 1996, Wray et al. estimated molecular clock rates based on differences in DNA in gnathostome vertebrates that diverged at known times in the fossil record. Because vertebrates and cephalochordates have very slow rates of DNA change, Wray et al. estimated that vertebrates diverged from all invertebrates one billion years ago (1 Ga) and from arthropods 1.2 Ga.[1] Other studies calculated similar divergence times. [2] Peterson et al. found that vertebrate rate of DNA change is approximately half that of Drosophila melanogaster and other invertebrates. Thus, he calculated the same ancient divergence time as that calculated by Wray and others.[3] The problem is that scientists do not know what the rate of change would be prior to the first appearance of vertebrates in the fossil record. The rate could have changed dramatically. Although vertebrates have DNA repair mechanisms that prevent mutation of DNA, invertebrate protostomes do not have these repair mechanisms and thus have much faster rates of change of DNA; thus, molecular clocks based on the rate of change of invertebrate DNA lead to last common ancestor calculations that are in line with initial animal divergence at the base of the Cambrian. Peterson thus proposed that the rate of vertebrate DNA change might have been rapid in the preCambrian and may have slowed since then.
In 2011[4] and 2015,[5] Erwin et al. calculated molecular clock rates based on genes across protostomes and deuterostomes. Erwin’s new calculations resulted in an estimate of the divergence between cnidarians and bilaterians at 700 Ma.
“The study included 24 different calibration points distributed across the tree, in contrast to the dominantly vertebrate calibration points used in previous studies, and employed a relaxed clock analysis…First, the results suggest an origin of Metazoa during the Cryogenian, approximately 780–800 Ma, the LCA of cnidarians and bilaterians at approximately 700 Ma and of bilaterians approximately 688 Ma (all estimates have analytical uncertainties discussed in detail in reference).” [6]
Paleontologists are becoming much more confident in the fossil and trace fossil record of cnidarians, bilaterians, and other animals in the Late Ediacaran and Early Cambrian (first few million years). There is excellent soft body preservation in the Ediacaran; thus, it is unlikely that paleontologists have missed the early evolution of phyla such as arthropods, annelid worms, or mollusks in the Ediacaran period. Simple worms evolved by the beginning of the Cambrian (542 Ma), and several of the major invertebrate phyla appear in the fossil record over the next 20 million years, with mollusks appearing earlier than others, as described in chapter 8. The similarity in genomes between the arthropods, annelid worms, mollusks, and deuterostome cephalochordates might indicate that they evolved alongside each other during the early Cambrian and diverged at various points in this 20 million year period; however, there is limited fossil information between the early Cambrian and the Chengjiang Lagerstatten. There is extensive fossil preservation in the few million years after the beginning of the Cambrian and at the point of the Chengjiang Lagerstatten and Burgess Shale, but limited preservation in between those two time points. Thus, the specifics of the evolution of and relationships between phyla after the beginning of the Cambrian is still a mystery.
The following debate focuses on the difference between the Precambrian and Cambrian fossil record and estimates of vertebrate origins with molecular clocks. Participants include a molecular clock expert (Phillip Donoghue), Cambrian and Precambrian paleontology (Alison Daly), genetics (Peter Holland), and Precambrian microorganisms and geochemistry (Rosalind Rickaby).
In his introduction, Phillip Donoghue argued for a deep time divergence of animals based on the molecular clocks, but he is also a fossil expert and made the following statement after the moderator asked him if the Cambrian explosion was real.
“I work on a fossil deposit that is within three million years of the base of the Cambrian (after the beginning of the Cambrian), and it has mollusks, various groups of pan arthropods, as well as cnidarians and other lineages, and it seems that you can fit all of animal evolution into that three million years, but then you go into the Precambrian, and there are various fossils that go back to 575-80 that many people believe are representative of the earliest branches of animal evolutionary history (Avalon Explosion), but the fossil record is silent about what goes on in between, and to me it’s a philosophy or a paradigm that it all has to be fit into the Cambrian. I don’t really see why that has to be the case, to me the fossil record begs that there is a prehistory, but being a fossil fondler, I do worry about the fact that I don’t find any animal fossils in the Ediacaran, or at least early bilaterians, and indeed I have spent the last 15 years basically going from one fossil group to another proving that there are no bilaterians or animals in the Ediacaran so it’s hard.”
In summary, Dr. Donoghue stated that he spent the last 15 years looking for bilaterian animals in the Precambrian, and he has found none, not even any flatworms or other possible animal ancestors. The moderator then asked Alison Daly (paleontologist) if there is missing animal evolution in the fossil record. She stated.
“There is still a fairly immense amount time we are dealing with here. Did animals evolve exactly at the base of the Cambrian at 541? It could go back say as far as 550 and what we see looking at the trace fossils and small shelly fossils, we see an increase in complexity that’s taking place in the bottom 20 million years of the Cambrian so if it’s from 550 till the time that we see complex ecosystems already in the first Burgess shale biota to the Chengjiang at 518, we’re still talking about 30 million years of time. It’s a lot of time for evolution to take place. Indeed, I don’t think that animals could evolve at 680 million years, and then we don’t see phyla until the Cambrian. Phil showed molecular clocks that suggest the phyla all appeared in the Cambrian, which I think we sort of agree with and everything you said about the rock record when you started is simply true. We have amazing preservation windows in the Ediacaran, and we don’t see convincing evidence of animals everywhere. It’s not a lack of rocks, and it’s not a lack of fossils. Molecular clocks inspired us (us being the broader us of paleontology and geology as a community) to really search in Ediacaran rocks and look for any evidence of animal life. Time and time again, the windows were open and animals aren’t being preserved, and if early animals that hadn’t yet evolved into phyla that we can recognize today were around, even if they were small or soft-bodied or huge and mineralized, all those windows are open and we just don’t see them in the rock record.”
Alison Daly also pointed out that preservation of soft tissues was very good in the Precambrian because there were no animals to disturb the dead soft-tissue organisms or disturb the environment in which there were preserved. There were no three-dimensional animals digging into and disturbing the sediment. She stated that soft-tissue preservation is why we can read the Precambrian fossil record close to literally. Rosalind Rickaby also stated that with lower oxygen, you would have better preservation. Phillip Donoghue argued that animals probably evolved from flatworms in the Ediacaran, and flatworms are not preserved at all as they decay.
Alison Daly stated that molecular clocks are constrained by fossils, so they are not completely independent of the fossil record. She published a paper in which the molecular clock worked well for arthropods. She stated that there are no calibration points for a molecular clock prior to the Cambrian Period. Peter Holland stated the following with respect to the vertebrate molecular clock,
“We are left with a bit of a dilemma because the fossil record just doesn’t quite look like the timings in those clocks to my mind.”
Phillip Donoghue admitted that there was disagreement, but that motivated him to do further research and not give up.
“I am uncomfortable with the relationship between the fossil record and what molecular clocks tell us but that’s science isn’t it. You know, we can deal with two incompatible bits of data and that prompts me to do new research.
Dr Rickaby stated that what is really needed is a Chengjiang Lagerstatten or Burgess Shale dated at 530 Ma in order to fill in the gap between the beginning of the Cambrian and the Chengjiang biota.
If the urbilaterian lived no earlier than 540 Ma, which is a reasonable estimate based on current knowledge of the fossil record and similarities between protostomes such as annelids and chordates, then this would constrain the time during which the vertebrate characteristics could evolve.
[1] Wray, Gregory A., Jeffrey S. Levinton, and Leo H. Shapiro. "Molecular evidence for deep Precambrian divergences among metazoan phyla." Science 274, no. 5287 (1996): 568-573.
[2] Peterson, Kevin J., Jessica B. Lyons, Kristin S. Nowak, Carter M. Takacs, Matthew J. Wargo, and Mark A. McPeek. "Estimating metazoan divergence times with a molecular clock." Proceedings of the National Academy of Sciences 101, no. 17 (2004): 6536-6541.
[3] Peterson, Kevin J., Jessica B. Lyons, Kristin S. Nowak, Carter M. Takacs, Matthew J. Wargo, and Mark A. McPeek. "Estimating metazoan divergence times with a molecular clock." Proceedings of the National Academy of Sciences 101, no. 17 (2004): 6536-6541.
[4] Erwin, Douglas H., Marc Laflamme, Sarah M. Tweedt, Erik A. Sperling, Davide Pisani, and Kevin J. Peterson. "The Cambrian conundrum: early divergence and later ecological success in the early history of animals." Science 334, no. 6059 (2011): 1091-1097.
[5] Erwin, Douglas H. "Early metazoan life: divergence, environment and ecology." Philosophical Transactions of the Royal Society B: Biological Sciences 370, no. 1684 (2015): 20150036.
[6] Erwin, Early metazoan life.
Wall clocks. Credit: Gausanchennai. Used here per CC BY-SA 4.0