Pharyngula

Doushantuo embryos dethroned?

Almost ten years ago, there was a spectacular fossil discovery in China: microfossils, tiny organisms preserved by phosphatization, that revealed amazing levels of fine detail. These specimens were identified as early animal embryos on the basis of a number of properties.

  • The cells were dimpled and shaped by adjoining cells, suggesting a flexible membrane—not a cell wall. This rules out algae, fungi, and plants.
  • The number of cells within each specimen was usually a power of 2. This is something we typically see in cleaving embryos, the sequence from 1 to 2 to 4 to 8 to 16 cells.
  • They were big. Typical somatic cells in animals are 5-10 µm in diameter, but ova can be a millimeter or more in diameter, and individual blastomeres (the cells in the cleavage stage embryo) can be several hundred µm across. These cells and the whole assemblage were in that size range.
  • The individual cells were uniform in size, as seen in many cleavage stage embryos, and contained organelles arranged in a consistent pattern.
  • They were often found encapsulated in a thin membrane, similar to the protective membrane around embryos.

There are some concerns about the interpretation, though. One troubling aspect of their distribution is that they are all only in the cleavage stage: we don’t see any gastrulas, the stage at which embryonic cells undergo shape changes and begin to move in a specific, directed manner. Studies of taphonomy (analyses of the processes that lead to fossilization) have shown that these later stages are particularly difficult to preserve, which potentially explains why we’re seeing a biased sample. Another unusual bias in the sample is that all of the embryos exhibit that regularity of division that produces equal-sized blastomeres—yet many invertebrate embryos have early asymmetric cleavages that produce recognizable, stereotyped distributions of cells. That asymmetry could be a feature that evolved late, but at the same time, some of the fossils were described as resembling molluscan trefoil embryos. Why aren’t the examples of early asymmetry translated into a later asymmetry?

Now there’s another reason to question the identity of the Doushantuo microfossils: they may be bacterial.

Bailey et al. have pointed out some stunning similarities between the phosphatized Doushantuo microfossils and sulfur-oxidizing bacteria of the genus Thiomargarita. They are of approximately the same size, form colonies of uniformly sized individuals that are the product of cell division and are in numbers that are powers of two, and now, suddenly, it seems that quite a few of the parameters of the fossils that were thought to be diagnostic of an animal embryo are much more ambiguous. Look for yourself: Thiomargarita is in the left column, representative microfossils on the right.

i-ca94fb82d55a9ee90e4233a09d7b21e8-bact_fossils.jpg
a, Solitary Thiomargarita cell from the Gulf of Mexico (after ref. 2). b, Two-cell cluster of Thiomargarita. c, Three-cell Thiomargarita cluster, thought to result from the incomplete division of a two-cell cluster. Greek letters identify each of the three cells. d, Tetragonal Thiomargarita tetrad resulting from reductive division in two planes. e, Offset between opposing cells in rhomboidal Thiomargarita tetrads resembles offset in some Doushantuo tetrads and cross-furrows in four-cell blastulas. Arrows indicate thin sheath surrounding cell cluster. a’, Megasphaera inornata, from the Doushantuo Formation. b’, Two appressed hemispherical bodies enclosed by an external envelope. c’, Thiomargarita triplets occasionally result from incomplete division, which results in two cells with a combined volume roughly equal to the third undivided cell. This Doushantuo globular triplet shows similar relative volumes. d’, Parapandorina tetrad resulting from division in two planes. e’, Doushantuo rhomboidal tetrad. Scale bars, 150 µm (b’); 100 µm (a?e, a’, c’?e’).

It doesn’t disprove their identification as embryos, but it does provide a strong alternative explanation that we will have to consider in any interpretation. In addition, these sulfur-oxidizing bacteria promote chemical reactions that can precipitate phosphates, generating the very conditions that preserve them so well. These conditions would also help preserve other organisms in the neighborhood, so it could be the case that what we’re seeing is a cloud of large bacteria that make a matrix that preserves other organisms—like, perhaps, some embryos.

As I’ve said before, I love the idea of being able to see 580 million year old embryos. Should I be disappointed at learning that perhaps these fossils are not of embryos?

Why, no.

I like reality and evidence. If further data demonstrate that not one of these fossils is a metazoan embryo and that all of them are interesting and unusual examples of large, specialized bacteria, that will be cool in a different sort of way. We follow where the evidence leads us, not where our predispositions want us to go.

Besides, there is one other fascinating part of this alternative explanation. The idea that the morphology of assemblages of bacteria might be superficially indistinguishable from the attributes of early metazoan embryos further blurs the line between the single-celled and multicellular worlds—the transition becomes even less difficult to explain. The basic principles of early development are not unique or miraculous or abrupt, they are extensions of molecular strategies pioneered in bacteria.


Bailey JV, Joye SB, Kalanetra KM, Flood BE, Corsetti FA (2006) Evidence of giant sulphur bacteria in Neoproterozoic phosphorites.
Nature advance online publication 20 December 2006.

Comments

  1. #1 llewelly
    December 23, 2006

    I’m wondering if perhaps they’re transitional fossils?

  2. #2 juju-quisp
    December 23, 2006

    This is just another example of the failure of the religion of Darwinism. Evolution is dead. Just admit it. You’ll be happier.

    I’m just kidding. Very cool read, PZ. I really do love the hard science on this blog even though I’m not a biologist. I always liked the little bit of this stuff we would get in medical school, though.

  3. #3 spudbeach
    December 23, 2006

    Wow! I’m a high school physics teacher, trying to get my students to act like scientists, and not blindly accepting everything their teachers say. I’m going to give them this example in the next class, showing them that no matter how much evidence there is supporting a hypothesis or a theory, there could always be more evidence somewhere that changes everybody’s mind.

    Should our students learn to question evolution? Of course — and they should learn to question Newton, Maxwell, Einstein and Genesis as well. I just have to be careful how I ask them to question that last one . . .

  4. #4 Ian Menzies
    December 23, 2006

    I want to be right. That’s why I love being proved wrong, because that means that I wasn’t right, but now I am.

  5. #5 Tom Foss
    December 23, 2006

    Should our students learn to question evolution? Of course — and they should learn to question Newton, Maxwell, Einstein and Genesis as well. I just have to be careful how I ask them to question that last one . . .

    That’s easy, just ask them “if she has an invisible touch, and it has no measurable effects on the natural world, isn’t it the same as if the touch didn’t exist at all?”

    Or, better yet, “who’s better, Peter Gabriel or Phil Collins?”

    They’ll be questioning Genesis in no time.

  6. #6 The Science Pundit
    December 23, 2006

    Very good explanation, indeed. That last paragraph really says a lot. I was thinking along those lines (though not as eloquently) when I read about this discovery a couple days ago in ScienceDaily.com. People tend to fall into the trap of thinking that human invented classification systems represent some fixed reality.

    A similar sentiment was expressed by Robert Hazen in his NewScientist article “What is Life?” last month.

    In spite of such well-intentioned efforts to define life, any attempt may be doomed to failure for the simple reason that the transition from the non-living to the living world was inherently gradual.

    To pin down the exact point at which such a system of gradually increasing complexity becomes “alive” is intrinsically arbitrary. “What is life?”, then, is fundamentally a semantic question. Nature holds a rich variety of complex chemical systems, and scientists increasingly are learning to craft such systems in the laboratory. Yet no matter how curious or novel their behaviour, none comes with an unambiguous label: “life” or “non-life”.

    When you start looking, you see this kind of thing in virtually every branch of science (what is a planet?)

    That is the complete opposite of the creationist mindset.

  7. #7 Monado
    December 23, 2006

    When I read about these microfossils a year or so ago, I thought that there must be a stage in the development of life as a whole when the most advanced thing on the planet would be embryos. They would have to develop and live as assemblages before they could invent the next stage of life — more cell layers, rudimentary circulation, or whatever. So in an odd way, ontology does recapitulate the ancient story.

  8. #8 truth machine
    December 23, 2006

    So in an odd way, ontology does recapitulate the ancient story.

    You’re being circular. Your belief that embryos must have been a “stage in the development of life” is based on taking the above conclusion as an implicit assumption. You’re making the same sort of mistake Behe makes in his IC arguments, assuming that evolution proceeds by a strict increase in complexity, each new system being an old system with something tacked on. But that isn’t how it works.

  9. #9 Jonathan Badger
    December 23, 2006

    Well, it’s not *impossible* that these cells were bacterial, and even bacteria like Thiomargarita (mmmm, sulfury tequilla…)

    But — here’s the deal — morphological similarities at the microscopic level really aren’t that informative. That’s why microbial systematics didn’t really get started until sequence data was available and people had more to work on than shape.

  10. #10 Fossilboy
    December 24, 2006

    “But — here’s the deal — morphological similarities at the microscopic level really aren’t that informative.”

    That’s true, but at this point, morphological similarities are no more useful for the embryo interpretation than they are for the bacterial interpretation. The other important aspect of the Bailey et al. paper deals with taphonomy (the conditions under which biological remains are preserved as fossils). This aspect of paleontology is often overlooked by biologists, but can have important implications for interpreting fossil remains and understanding ancient life. In this case, the Doushantuo microfossils are preserved in phosphorites. Modern Thiomargarita cells, as part of their metabolism, concentrate and release copious amounts of phosphate, which results in the precipitation of abundant phosphatic minerals. It’s not *impossible* that millions of animal embryos ended up in an environment where phosphorites were forming, and for whatever reason never made it past early cleavage stages, but a more parsimonious explanation is that these microfossils are simply fossilized Thiomargarita cells preserved in their natural habitat.

  11. #11 truth machine
    December 24, 2006

    a more parsimonious explanation is that these microfossils are simply fossilized Thiomargarita cells preserved in their natural habitat

    Ain’t that a fact.

  12. #12 brightmoon
    December 26, 2006

    Thiomargarita

    sulfur pearls?

    “Modern Thiomargarita cells, as part of their metabolism, concentrate and release copious amounts of phosphate, which results in the precipitation of abundant phosphatic minerals.”

    sulfur phosphates?..(just curious )..do they turn into other phosphate minerals or are they secreted by the cells as sulfur minerals or other phosphates ..wouldnt these have obvious accretion layers if they were thio margarita balls ?

    i wish i knew more geology than i do

    /

  13. #13 Michael Buratovich
    December 26, 2006

    PZ,

    The giant bacteria all have somewhat stereotypical ways of dividing. It could be that the selective pressure that probably leads to huge sizes in bacteria – avoidance of predation by larger eukaryotes, was also around ~600 million years ago.

    It seems to me that more work is needed. These fossils could be bacterial, but they might also be genuine fossilized embryos. It seems to me that the jury is still out.

    MB

  14. #14 Joe Meert
    December 26, 2006

    This is not new(s). The lagerstatte (in spite of these problematica) is no less a resource for the early evidence of bilaterians and precursors to the Cambrian expansion:

    The two main spherical microfossils, Megasphaera and Parapandorina, have been described as animal eggs and cleavage-stage embryos, respectively (Shen et al., 2000). The interpretations of other microfossils are not so certain, however (Shen et al., 2000). One of the controversies surrounding the Doushantuo embryos is that no gastrulas or adult animals have been found (Shen et al., 2000). This could be due to the animals travelling to the upper water column after the embryo stage, or maybe sediment reworking that sorted fossils by size (Shen et al., 2000).

    Cheers

    Joe Meert

  15. #15 Fossilboy
    December 27, 2006

    “This is not new(s). The lagerstatte (in spite of these problematica) is no less a resource for the early evidence of bilaterians and precursors to the Cambrian expansion”

    The metazoan origins of other Doushantuo microfossils have all been contested because the features establishing their metazoan origins could easily be diagenetic artifacts (Xiao 2000, Bengston and Budd, 2004, Zhang et al., 1998 etc.). Parapandorina and Megasphaera were widely accepted because of the lack of serious alternatives (algae don’t meet the combined criteria of 1) large size 2) reductive division 3) deformable cell walls/membranes). The jury is still out, but until this paper, there were no reasonable alternatives – so at this point all the other Doushantuo microfossils have non-metazoan alternative explanations. Hence, it is currently a questionable resource.

    “This could be due to the animals travelling to the upper water column after the embryo stage, or maybe sediment reworking that sorted fossils by size (Shen et al., 2000).”

    Or it could be because they are actually bacteria as Bailey et al., hypothesize. What makes the “embryos” magically travel to the upper water column after reaching 128 cells, rather than forming a blastocoel? Sedimentological sorting is argued against in the Bailey et al. supplement.

  16. #16 Fossilboy
    December 27, 2006

    “The giant bacteria all have somewhat stereotypical ways of dividing.”

    As far as I know, that’s not correct. Kalanetra et al. were the first to describe reductive division (constant volume), as opposed to fission (increased volume), in this particular species of Thiomargarita. If you have a different example, please cite the literature. Epulopiscium is a different kind of giant bacterium that lives in fish intestines – it produces multiple active intracellular offspring, which is also very interesting. Lots still to learn in the microbial world folks.

    “It seems to me that the jury is still out.”

    Yes, that’s true – but it’s likely news to most people that the case isn’t closed.

  17. #17 Truman
    April 8, 2007

    I had just came accross this paper. I don’t know if its old news already.

    “Phosphatized microfossils in the Ediacaran (635-542 Myr ago) Doushantuo Formation, south China, have been interpreted as the embryos of early animals. Despite experimental demonstration that embryos can be preserved, microstructural evidence that the Doushantuo
    remains are embryonic and an unambiguous record of fossil embryos in Lower Cambrian rocks, questions about the phylogenetic relationships of these fossils remain. Most recently, some researchers have proposed that Doushantuo microfossils may be giant sulphur-oxidizing bacteria comparable to extant Thiomargarita sp. Here we report new observations that provide a test of the bacterial hypothesis. The discovery of embryo-like Doushantuo fossils inside large, highly ornamented organic vesicles (acritarchs) indicates that these organisms were eukaryotic, and most probably early cleavage stage embryos preserved within diapause egg cysts. Large acanthomorphic microfossils of the type observed to contain fossil embryos first appear in rocks just above a 632.5 +/- 0.5-Myr-old ash bed, suggesting that at least stem-group animals inhabited shallow seas in the immediate aftermath of global Neoproterozoic glaciation.”
    Yin L, Zhu M, Knoll AH, Yuan X, Zhang J, Hu J., Nature. 2007 Apr 5;446(7136):661-3.

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