Deciphering the fossil record of early bilaterian embryonic development in light of experimental taphonomy

Abstract

Experimental analyses of decay in a tunicate deuterostome and three lophotrochozoans indicate that the controls on decay and preservation of embryos, identified previously based on echinoids, are more generally applicable. Four stages of decay are identified regardless of the environment of death and decay. Embryos decay rapidly in oxic and anoxic conditions, although the gross morphology of embryos is maintained for longer under anoxic conditions. Under anoxic reducing conditions, the gross morphology of the embryos is maintained for the longest period of time, compatible with the timescale required for bacterially mediated mineralization of soft tissues. All four stages of decay were encountered under all environmental conditions, matching the spectrum of preservational qualities encountered in all fossil embryo assemblages. The preservation potential of embryos of deuterostomes and lophotrochozoans is at odds with the lack of such embryos in the fossil record. Rather, the fossil record of embryos, as sparse as it is, is dominated by forms interpreted as ecdysozoans, cnidarians, and stem-metazoans. The dearth of deuterostome and lophotrochozoan embryos may be explained by the fact that ecdysozoans, at least, tend to deposit their eggs in the sediment rather than through broadcast spawning. However, fossil embryos remain very rare and the main controlling factor on their fossilization may be the unique conspiracy of environmental conditions at a couple of sites. The preponderance of fossilized embryos of direct developers should not be used in evidence against the existence of indirect development at this time in animal evolutionary history.

Embryo fossilization is a biological process mediated by microbial biofilms

“…1 A and B) that resemble Neoproterozoic and Cambrian fossil embryos in general features of cell morphology and size (10). Our results illuminate the processes of decay, preservation, and mineralization of animal embryos, as well as biases in preservation that may influence interpretations of developmental mode (10)(11)(12).…”

“…The frequency of these mineralization modes remains to be determined for embryos. However, all fossil embryos show evidence of decay and, in the vast majority of cases, decay has been so considerable that only gross features such as the fertilization envelope or other outer coverings remain (12,13,29). Thus, embryo fossils are, to a greater or lesser degree, microbial pseudomorphs of the original cells and this fabric can be seen replicated in mineral.…”

“…1C). Thus, for fossilization of embryo structures to occur, the conditions for fossilization must block autolysis, which experimentally can be prevented by reducing conditions (produced by addition of 100 mmol of ␤-mercaptoethanol) (11,12), or anaerobic conditions (see Materials and Methods). Evidence that compatible conditions obtained during the initial stages of metazoan fossilization is apparent in the sediments from which fossilized embryos have been recovered (13).…”

“…We show that embryo taphonomy is the product of 3 distinct processes. First, and most rapid, is autolysis, the selfdestruction of cells within hours under aerobic conditions by their own lytic enzymes (11,12). Thus, preservation sufficient for potential fossilization with preservation of tissue and cell structure requires that there were conditions in ancient marine environments that provided a rapid block to autolysis on death of the embryo.…”

Experimental mineralization of crustacean eggs: new implications for the fossilization of Precambrian–Cambrian embryos

“…Recent studies focused on the factors, which affect the decay and preservation of the earliest stages on embryonic and larvae development (Gostling et al, 2008(Gostling et al, , 2009Raff et al, 2006Raff et al, , 2008. Four stages of decay can be distinguished (Gostling et al, 2008): (a) The onset of autolysis, (b) some shrinkage within the fertilization envelope, enzymatic breakdown of the cyctoplasm and coalescence of sub-cellular lipids, often associated with the degradation of cell structures through the activity of endogenous and exogenous microbes (cf. Raff et al, 2006), (c) continued degradation of cell structures and breakdown of the fertilization envelope, (d) generation of amorphous organic matter due to the total breakdown of subcellular material.…”