The Cambrian Whimper? An Interview with John Moore

 A.C. Maloof, S. M. Porter, J. L. Moore, F. O. Dudas, S. A. Bowring, J. A. Higgins, D. A. Fike, M. P. Eddy. The earliest Cambrian record of animals and ocean geochemical change. Geological Society of America Bulletin, 2010; 122 (11-12): 1731 DOI: 10.1130/B30346.1

The Cambrian “explosion” of animals is considered one of the most puzzling phenomena in the fossil record. I know it’s a little clichéd to include a quote the Encyclopedia Britannica, but I feel their definition captures the average sentiment of what the Cambrian explosion is; not as nuanced as you would get from a specialist, and not as mistaken as I have seen on some creationist websites:

“Cambrian explosion: the unparalleled emergence of organisms between 542 million and approximately 530 million years ago at the beginning of the Cambrian Period. The event was characterized by the appearance of many of the major phyla (between 20 and 35) that make up modern animal life.”

It is sometimes phrased as “all major groups of animals” appearing “suddenly” during this time period.  There are two things in particular that bother me about this definition. While it’s not entirely wrong, it is worth breaking this definition down, since the Cambrian explosion is commonly misunderstood by scientists and non-scientists alike:

1) First of all, when scientists talk about the appearance of the “major phyla”, they mean that the first members of the different animal bodyplans evolved.  For example, although there is no evidence of squid or octopus in the Cambrian, there were animals that shared their basic mollusc bodyplan (for more details on the molluscan bodyplan, see the post “How to Build a Snail”). Whether “the bodyplan” or “phylum” has any real scientific meaning is still debated, and is a big topic in evo-devo research.

So to be clear, there were no humans in the Cambrian. In fact, there were no mammals at all.  There were no birds, reptiles, amphibians, or fish.  There were no insects, starfish, or sea urchins.  Almost all of the animals that people think of evolved millions of years after the Cambrian.

2) My second concern is with the description of evolution in the Cambrian as, rapid, sudden, or an explosion. The Cambrian period lasted over 40 million years. And although many animal groups make their first fossil appearance in the Cambrian, they did not all do so at the same time.  While the Encyclopedia Britannica suggests that animals radiated between 542 and 530 million years (which would still be a 12 million year period), new discoveries in the fossil record have pushed many of those dates further back.  Mollusc shells (Helcionellids) are known from 540 million years ago, and the probable mollusc Kimberella dates back to 555 million years ago.  There are unarguable sponge fossils that date back 580 million years, and there is chemical evidence for sponges in the rock record going back 1,800 million years. There were also many animals, including Spriggina, Dickensonia, and Yorgia, which evolved well before the Cambrian.  Even though it is difficult to determine which animal phyla these creatures belonged to, it is clear that animals did not suddenly appear from nowhere.

In this vein, Maloof et al. did a worldwide dating and calibration of early Cambrian rocks.  These scientists used multiple isotope dating methods (including Uranium/Lead dating, Strontium dating, and Organic and Inorganic Carbon curves) to sync up the dates between the different Cambrian deposits.  Isotope dating provides absolute dates on rocks, and avoids the potential circularity of arguing that rocks are of the same age because they have similar fossils, then arguing that those fossils first appear in rocks of the same age.

Mallof et al. discovered that the evolution of at least some Cambrian animals occurred slower and over a longer period of time than many geologists have previously thought.  This work pushes the origination of small, shelly animal fossils from the Cambrian’s Tommotian Age (530 million years ago) to the Nemakit-Daldynian Age (540 million years ago).  They also argue that the expansion of these animals happened in three evolutionary “pulses” as opposed to a single “explosion”

I talked to one of the authors of this paper to find out more about the implications of this work.  John Moore is working with Dr. Susannah Porter at the University of California, Santa Barbara, on the small shelly fossils of the Cambrian.  Below are some questions he was kind enough to answer about this interesting study:

How would you define small shelly fossils, and what is their importance to understanding animal evolution?

Moore: "Small shelly fossil" is a term conventionally given to any small biomineralized fossil obtained from rocks from the Lower Cambrian (or occasionally from slightly younger rocks). They are most commonly preserved by calcium phosphate (either because that was their original composition or, more commonly, because fossils that were originally calcium carbonate have become filled or coated with phosphate) and are hosted in a limestone or dolostone, and are consequently easily isolated from their host rocks by dissolving them in dilute acid. As a result, small shelly fossils are united on the basis of a style of preservation rather than any biological relationship. From a taxonomic perspective, small shelly fossils are a very heterogeneous assemblage.

Small shelly fossils are important for several reasons. While there are a few biomineralized animals known from the Ediacaran (such as Cloudina), the small shelly fossils record the first time when animals with hard parts really became diverse and abundant. They're also fascinating simply because for the first 20 million years or so of the Cambrian, they are one of the most important records we have of animal evolution.

Do we understand how the small, shelly fossils relate to specific clades of living animals?  Are they related at all?

Moore: As mentioned above, small shelly fossils are a very heterogeneous assemblage: some can be related to particular modern groups, and some can't. Mollusc shells and sponge spicules are sometimes considered small shelly fossils, and an increasing number of formerly problematic forms can be placed phylogenetically: for example, there are small shelly fossils that are probably cnidarians, chaetognaths, ecdysozoan worms, stem-group panarthropods, stem-group brachiopods, among others. There are still many small shelly fossils whose affinities remain mysterious, however!

Do you have any personal opinions on whether the three pulses of small, shelly fossils are most likely to be real versus biases in the fossil record?

Moore: The observation of the same pulses on separate paleocontinents suggests that they had some sort of global cause, but I don't know whether that was due to evolution of new animals or to global preservational biases (such as might be caused by changing sea levels), or both.

In this paper, you distinguish between an increase in diversity (the number of organisms), and disparity (how physically different those organisms are from each other).  If high disparity during an evolutionary radiation is not unusual, and you have minimized the rapid, sudden increase in diversity, is there a “Cambrian explosion” left?

Moore: I guess I don't particularly care for the expression Cambrian "explosion," as it would seem to imply an event that is far more inexplicable than I think is actually the case. There's no doubt that the Early Cambrian still remains one of the most important and dramatic times in the history of life on Earth, however: there's such a great diversification of animals, with so many important clades and new characters appearing for the first time, and animals also become so much more dominant ecologically (for example, you see a change from a regime in which sedimentary processes are controlled by microbes to one where there is a strong animal impact).

How to Build a Marsupial

A. L. Keyte, K. K. Smith. Developmental origins of precocial forelimbs in marsupial neonates. Development, 2010; 137 (24): 4283

Marsupials—kangaroos, koalas, wombats, and their relatives—are an exotic group of mammals. This is partially because, unless you live in Australia, you’re unlikely to see many outside of a zoo.  But marsupials are also unique because of their mode of development.  Most mammals are eutherians, or mammals with placentas. The placenta is an organ that connects a fetus to the uterus of its mother, allowing for the exchange of nutrients and waste. This means babies can develop for a longer period of time inside the mother than other animals (if you’re an elephant, this can be as long as 60 months).  Marsupials lack a placenta; so their offspring are born much earlier than eutherian mammals.  So without any help from the mother, the newborn has to migrate to the mother’s pouch, where it can suckle milk and continue development.

The reason that marsupial newborns can accomplish this is that they have unusually strong and well-developed forelimbs. Below are the images of a newborn mouse (a eutherian) on the left and a newborn opossum (one of the only non-Australian marsupials) on the right.  Even though the newborn opossum is at a much earlier stage of development, the arms are similar in proportion to the mouse:

In a recent issue of the journal Development, Keyte and Smith set out to find whether changes in the timing of genes might correlate with the early development of marsupial forelimbs.  They compared the development of the opossum Monodelphis domestica with the mouse Mus musculis, looking at a number of genes known to be important to limb development. This included the limb-patterning gene Sonic Hedgehog (shh), forelimb gene T-box 5 (Tbx5), hindlimb gene T-box 4 (Tbx4), and the Tbx downstream targets, fibroblast growth factor 10 (Fgf10) and 8 (Fgf8).  When Keyte and Smith synched up the two animals development, they discovered that almost all of these genes are turned on earlier in the opossum than in the mouse (in the figure below the term “FL” before the gene name implies expression of the gene in the forelimb, while “HL” means gene expression in the hindlimb):

In addition to changes in the timing of gene expression, there is also early movement of nerve cells and myocites (primitive muscle cells) into the limb bud.  Although it might seem like a lot of changes have to occur to create this advanced forlimb, the authors argue that most of the observed changes can be explained by a single event.  A change in the timing (or heterochrony) of Tbx5 expression would lead to early expression of Fgf10 since Tbx5 is known to regulate Fgf10. Fgf10 controls expression of Fgf8, so a mutation that turns Tbx5 on early will set the whole cascade of the gene network going.  The developing forelimb bud itself encourages the migration of nerves and myocites into the limb, creating a complex foreleg early in development.  Thus, a few small changes can have a large affect on the growth of the animal limb.

It might seem initially surprising that genes in the hindlimb also turn on earlier in opossum than in mouse, even though the opossum doesn’t also develop large, functional hindlimbs at birth. Since Tbx5 and Tbx4 are closely related genes, it is possible that the two are controlled by a similar upstream genes.  This would make it difficult (or perhaps impossible) to evolve early expression of forelimb genes without also patterning early development of the hindlimbs.  Such complications between forelimb and hindlimnb adaptation have been noted before.  In Stephen Jay Gould’s essay, “The Panda’s Thumb”, he notes how pandas have an elongated wrist bone (or radial sesamoid) to use as a false thumb to eat bamboo, but they have a similarly elongated bone (a tibial sesamoid) in their foot:

In a panda's foot, the counterpart of the radial sesamoid, called the tibial sesamoid, is also enlarged, although not so much as the radial sesamoid. Yet the tibial sesamoid supports no new digit, and its increased size confers no advantage, so far as we know…Repeated parts of the body are not fashioned by the action of individual genes—there is no gene "for" your thumb, another for your big toe, or a third for your pinky. Repeated parts are coordinated in development; selection for a change in one element causes a corresponding modification in others. It may be genetically more complex to enlarge a thumb and not to modify a big toe, than to increase both together.

Interestingly, it appears that the lack of hindlimb growth doesn’t come from a lack of gene expression.  Instead there simply aren’t enough cells in that region to provide the raw material necessary to build the hindlimb. The concept that there are tradeoffs regarding how many “traits” a body can build at once might deserve more consideration then it has gotten, but there are known examples.  For instance, some beetles that develop elaborate horns have reduced antennae, wings, or even eyes, because there simply isn’t enough cellular material and energy to build all of these things (e.g. Emlen and Costs 2001). Keyte and Smith note that the last gene in the hindlimb pathway Fgf8, is the only gene that does not turn on significantly earlier in the opossum than in the mouse.  This “pause” in the hindlimb gene network might be the result of a lack of cellular material, or be an additional cause of the normally developed hindlimb. 


Ultimately, like Osterauer et al. (see my post “How to Build A Snail”), this is a clear example of how a small change in development can have a large impact on an animal.  The only minor issue I had with it was its constant referral to how the development of the marsupial has changed so dramatically from the mouse.  But if you look at the evolutionary tree of mammals (I whipped one up below for you to look at), it seems most likely that placental mammals evolved from pouched marsupials, who evolved from egg-laying monotremes (and before that, reptiles).  So if anyone’s development has radically changed, it would be the mouse, and not the opossum.

Papers Cited

Emlen, D. J. (2001) Costs and the diversification of exaggerated animal structures. Science 291: 1534-1536.

Gould, S.J. (1980) The Panda's Thumb, New York: W. W. Norton, ISBN 0-393-01380-4

Tullio, A. N. Accili, D. Ferrans, V. J. Yu, Z. Takeda, K. Grinberg, A. Westphal, H. Preston, Y. A. Adelstein, R. S. (1997) Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc Natl Acad Sci USA 94:12407–12412