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

Homology in the Age of Evo Devo: Part 1

Last week, I got to catch a talk and spend some time with Nicholas Holland, a biologist from the Scripps Oceanographic Institute at UC San Diego.  Dr. Holland discussed the history of the “homology” concept in science. Today, I want to start with a primer on the current debates regarding homology, and a little bit about the history of the concept. 

A Homology Primer

The textbook definition of homology is simple: homologies are characters that are shared by two organisms because they both inherited that characteristic from a common ancestor.  For example, the reason that humans, cats, and hedgehogs all have fur is because they share a furry common ancestor. Fur is a homologous trait among mammals.

However, it is not always so easy to determine what characteristics are really homologous.  Humans have complicated eyes, and so do octopi.  Are these structures homologous?:

Some aspects of these eyes are similar, for example they both have a lens and a retina. But some other characteristics are quite different. Human eyes develop as outgrowths of the brain, while octopus eyes develop from invaginations of the animal’s surface.  In humans, nerve fibers pass in front of the retina, creating a blind spot, while in octopi, the nerve fibers are behind the retina, so they don’t have that same limit to their vision.  These many differences, combined with the fact that many relatives of humans and octopi lack complex eyes, has led most scientists to conclude that human and octopus eyes evolved independently, or that they are evolutionarily convergent.

And the concept gets further complicated by the fact homology can vary depending on what level of organization you are talking about.  For example, the wings of bats and birds are convergent; each has independently evolved wings from an ancestor that had forelegs.  However, at the skeletal level the wings of birds and bats are homologous; they share the same bones in their wings (such the humerus) because the last ancestor of these animals had the same bones in its forelimb:

Homologies can exist at the genetic level as well. In the 1960’s, before genetics was well understood, many prominent scientists thought that animals gain and lose genes too quickly during evolution for homologous genes to exist (Dr. Holland had a great quote from the prominent, and in this case very wrong, biologist Ernst Mayr, “the search for homologous genes is quite futile except in very close relatives”).  We now know that most genes important to development are shared in animals as diverse as humans, fruit flys, and jellyfish. This discovery has been critical to biology, earning the 1995 Nobel Prize in Physiology or Medicine, and leading to the birth of evo-devo, but it has really complicated the idea of homology. The genes Pax6, Eyes absent, sine oculis, and dachsund form a network that is critical not only to the eyes of humans and cephalopods like octopi, but also the compound eyes of insects, which look nothing like our “camera-type” eyes. In fact, these genes are so conserved, that if a mouse has a faulty version of any of these genes, scientists can “rescue” eye development by injecting the mouse with the fruit fly version of the gene! Some evo-devo scientists have called this “deep homology”; that at the level of genetics these structures are derived from the same ancestral gene networks (e.g. Shubin, Tabin, and Carroll 1997).

But what does deep homology really mean?  In the 90’s many scientists took a very literal view.  If two animals shared an “eye” gene like Pax6, then their last common ancestor must have had Pax6 as well, and therefore an eye.  Many papers were using shared genes to construct complex animal ancestors (e.g. Arendt and Nubler-Jung 1996, De Robertis and Sasai 1996).  Dr. Holland included a great image of this idea in his talk, which was taken from Veraska et al (2000).  This shows the complex ancestor of humans, octopi, and frut flies, and the genes used to justify the complexity:

In the last decade, this idea has become hotly contested.  Some animals that do not share these complicated structures do share these genes, and some animals with these complex structures do not use the same genes to build them.  Currently, there is no consensus about what homologous genes tell us about the physical nature of the common ancestor.  I think this is the biggest question in evo-devo today. In my next post, I’ll go into detail on how Dr. Holland tackles this problem.

Papers Cited

Arendt, D. and Nubler-Jung, K. (1996). Common ground plans in early brain development in mice and flies. BioEssays 18, 255-259

De Robertis, E.M. and Sasai, Y. (1996). A common plan for dorso-ventral patterning in Bilateria. Nature 380, 37-40.

Mayr, E. (1963) Animal Species and Evolution. Harvard Univ. Press (p. 609)

Shubin, N., Tabin, C. & Carroll, S. (1997). Fossils, genes, and the evolution of animal limbs. Nature 388, 639–648

Veraksa, A, Del Campo, M. and McGinnis, W. (2000). Developmental patterning genes and their conserved functions: From model organism to humans. Molec. Gen. & Metabolism 69: 85-100.

How to Build A Snail

Raphaela Osterauer, Leonie Marschner, Oliver Betz, Matthias Gerberding, Banthita Sawasdee, Peter Cloetens, Nadine Haus, Bernd Sures, Rita Triebskorn, Heinz-R. Köhler. Turning snails into slugs: induced body plan changes and formation of an internal shell. Evolution & Development, 2010; 12 (5): 474

Osterauer et al. recently published a paper in the journal Evolution and Development where they were able to radically change the bodies of adult snails ( Marisa cornuarietis ) by exposing embryos to the metal platinum.

Snails, along with slugs, clams, octopi, and squid, are part of the group Mollusca (unsure of where the molluscs fit into the animal tree? Check the reference phylogeny).  Molluscs share a basic bodyplan, although it has been highly modified in different groups.

Snails, for example, develop their shells through a bizarre developmental process called torsion.  During torsion, multiple parts of the body are rotated 180 degrees.  By the end, the anus and gills are sitting above the head of the animal, the nervous system has turned into a figure 8, and the right and left hand sides of the animals have become assymetrical:

While scientists don’t entirely understand why torsion occurs, it is related to the growth of the external shell and the muscles that attach to it.  In other species of molluscs, such as cephalopods (octopi, squid, cuttlefish), nudibranchs (sea hares), and pulmonate slugs, torsion never occurs.  Instead, the shell grows inside of the animal, creating a cone-shaped internal shell. The cuttlefish bone, which is often sold in pet stores as a calcium supplement for birds, is an example of this internal shell.

While trying to study the effects of certain toxic metals on the snail M. cornuarietis, Osterauer et al. found that exposure to platinum led some snails to loose their shells.  In this study, the scientists discovered that when M. cornuarietis embryos are exposed to a concentration of 164.4 milligrams of platinum per liter during the fourth and fifth days of development, the mantle tissue stays inside of the body (at this level of platinum, 100% of animals tested had this result).  In a normal snail, the mantle tissue moves to the outside of the animal, and is responsible for secreting the chemicals that harden into a shell.  In the image below, the edge of the mantle tissue is stained black and pointed out with an arrow; notice the difference between the normal snail embryo on the left and the platinum-exposed embryo on the right:

So instead of forming a normal shell, the shell developed within the body, like one might find in a squid or slug. These shells developed cone-like shapes that are reminiscent of those found in mollusks that lack external shells. Below are photos of adult shell-less snails, with images of their internal shells superimposed to show size and location:

Without normal shell-formation, the gills and mantle tissue stay in the posterior end of the animal like in other molluscs.  The gut, however, still goes through torsion, with the anus moving into the anterior region.

The fact that they recovered similar results from a second, distantly related snail, Planorbarius corneus, increases the possibility that the authors have discovered an important aspect of snail torsion, as opposed to an anomaly restricted to Marisa cornuarietis.

Here are the points I think are important in this paper:

1) This study does NOT suggest that platinum was responsible for the evolution of snails into slugs and cephalopods (or vice versa).

Because platinum is not having any effect on the DNA of the snails, they cannot pass these changes on to their offspring.  If a change is not heritable then it cannot be important to evolution in the long term. 

2) What this work does suggest is that a small change in development plays a huge role in the design of a snail.

The most important point of this paper is that one change, the position of the mantle tissue, affected many attributes of the snail, including the shape of the shell, the position of the shell and the position of the gills.  Instead of each of these characteristics having to evolve independently in the evolution of snails into slugs and cephalopods (or vice versa, the evolutionary history of the molluscs is still not well known), one change in development could affect all of these attributes at once.

While platinum exposure almost certainly was not responsible for this evolutionary change, the platinum is probably disrupting a gene network that is important to snail torsion.  If scientists can determine which gene(s) are involved in this change, they might discover how natural mutations in snail DNA led to the same results as the platinum exposure. Hopefully this work will be followed up on by these researchers.  In fact, Osterauer et al. already have an educated guess that the platinum might be disrupting a Calcium-based positioning system, although the authors did not find any significant difference in calcium uptake between experimental and control animals.