Taphonomy of fossilized embryos

There are these fossilized embryos from the Ediacaran, approximately 570 million years ago, that have been uncovered in the Doushantuo formation in China. I’ve mentioned them before, and as you can see below, they are genuinely spectacular.

Parapandorina raphospissa

But, you know, I work with comparable fresh embryos all the time, and I can tell you that they are incredibly fragile—it’s easy to damage them and watch them pop (that’s a 2.3MB Quicktime movie), and dead embryos die and decay with amazing speed, minutes to hours. Dead cells release enzymes that trigger a process called autolysis that digests the embryo from within, and any bacteria in the neighborhood—and there are always bacteria around—descend on the tasty corpse and can turn it into a puddle of goo in almost no time at all. It makes a fellow wonder how these fossils could have formed, and what kind of conditions protect the cells from complete destruction before they were mineralized. Another concern is what kinds of embryos are favored by whatever the process is—is there a bias in the preservation?

Now Raff et al. have done a study in experimental taphonomy, the study of the conditions and processes by which organisms are fossilized, and have come up with a couple of answers for me. Short version: the conditions for rapid preservation are fairly easy to generate, but there is a bias in which stages can be reliably preserved.

The experiments are straightforward. They worked primarily with embryos of the sea urchin Heliocidaris erythrogramma, as well as a number miscellaneous smaller species to test the effect of size, and killed them under various conditions and watched to see what would happen. There are two secrets to getting good embryo preservation: the animals have to be kept in anoxic, reducing conditions, and the fertilization envelope must be intact. The preserving conditions were generated by putting the embryos in a solution of sea water with 100 mM β-mercaptoethanol; this is analogous to immersing them in the H2S environment believed to have killed the Doushantuo specimens, without the nasty toxic risks of working with hydrogen sulfide in the lab. Photos A-C below show embryos kept in the β-ME solution for days to weeks, and while they are as dead as can be, the cells are still beautifully intact. D and E are embryos that were killed with β-ME, but then placed in pure seawater—the deterioration is obvious.

Cleavage-stage H. erythrogramma embryos under preserving and
nonpreserving conditions. (A and B) Embryos killed at the two-cell stage by
placing them in seawater containing 1% ammonium for 10 min, then trans-
ferring them to seawater containing 100 mM
after 2 (A) or 10 (B) days. (C) Embryo killed at the eight-cell stage by transfer
into seawater containing 100 mM
Embryos from the same two-cell stage culture as in A and B but returned to
normal seawater after killing, photographed after 2 days. Embryos have
undergone autolysis: cytoplasmic lipid and pigment have coalesced (arrows);
cleavage furrows have degraded (asterisks); and fertilization envelopes are
disintegrating (arrowhead). Autolysis is further advanced in the top embryo
than in the bottom embryo. In the bottom embryo, the process is further
advanced in the left-hand blastomere (arrow) than in the right-hand blas-
tomere. (E) Decaying surface of an embryo from the set shown in A and B,
returned to normal seawater after 4 days in reducing conditions, photo-
graphed 7 days later (total 11 days postdeath). Onset and progress of decay is
slower than autolysis in embryos never exposed to reducing conditions. The
fertilization envelope degrades and the cytoplasm of the embryo is then
exposed to external decay processes, including attack by protists (arrows).
(Scale bar: 200 µm A-D; 32 µm E.)

The reducing conditions of a β-ME solution would keep embryos intact for weeks, long enough for phosphatization to begin. The effect was independent of embryo size, too, with both small and large embryos being successfully preserved. That suggests that the relatively large size of the fossilized specimens may not be a preservation artifact, but may reflect the actual size distribution of Ediacaran embryos.

Unfortunately, there are serious biases in preservation. The fertilization membrane is a kind of spherical protein coat that surrounds newly fertilized embryos, forming a kind of shell within which the embryos develop. Without that membrane, the embryos disintegrate fairly quickly, even in the β-ME solution. That means that we’re unlikely to ever find post-hatching larva in these fossil layers—once they’ve emerged from that membrane, the conditions just don’t work to preserve their structure intact any more. In addition, the reducing conditions that work so well to preserve cell structure dissolve calcite skeletal elements, so skeletons and shells would also be lost. In addition, later stage embryos, where cell-cell adhesion is relatively weaker, are poorly preserved as the arrangements of the cells become scrambled.

Here is a summary of the results:

Consequences of death and postdeath conditions for
soft-bodied embryos
  Condition Outcome
Mode of death
  Fast Normal cell cleavage pattern
  Slow Abnormal cell cleavage pattern
Fertilization envelope present
  Normal seawater Rapid autolysis
  Reducing conditions Extended preservation
  Cleavage stages Cell arrangement retained
  Prehatching blastula Cell arrangement lost
Fertilization envelope absent
  Normal seawater Rapid decay
  Reducing conditions Rapid loss of morphology;
individual cells preserved

The positive answer from this work is that those Ediacaran fossil embryos probably are faithfully preserved, and represent a reliable picture of the distribution of embryonic characters over a broad range of phyla. The bad news, though, is that larvae wouldn’t have been preserved; the absence of feeding larvae in those formations doesn’t mean that they weren’t there, just that the conditions present wouldn’t have preserved them. From the Raffs’ other work, we know that one strong interest is in the evolution of direct- and indirect-developing forms, or life history evolution. We aren’t going to get the answers directly from fossil observations, I’m afraid, but they do hold out some hope that the presence of feeding larval stages can be inferred from indirect evidence, such as the size distribution of the embryos.

Raff EC, Villinski JT, Turner FR, Donoghu PCJ, Raff RA (2006) Experimental taphonomy shows the feasibility of fossil embryos. Proc Nat Acad Sci USA 103(15):5846-5851.