Comparative Review: The Phylotypic Stage of Vertebrates, Common versus Distinct Features, and Aspects of Evolution

A new and more robust evolutionary synthesis is emerging that attempts to explain macroevolution as well as microevolutionary events. This new synthesis emphasizes three morphological areas of biology that had been marginalized by the Modern Synthesis of genetics and evolution: embryology, macroevolution, and homology. The foundations for this new synthesis have been provided by new findings from developmental genetics and from the reinterpretation of the fossil record. In this nascent synthesis, macroevolutionary questions are not seen as being soluble by population genetics, and the developmental actions of genes involved with growth and cell specification are seen as being critical for the formation of higher taxa. In addition to discovering the remarkable homologies of homeobox genes and their domains of expression, developmental genetics has recently proposed homologies of process that supplement the older homologies of structure. Homologous developmental pathways, such those involving the wnt genes, are seen in numerous embryonic processes, and they are seen occurring in discrete regions, the morphogenetic fields. These fields (which exemplify the modular nature of developing embryos) are proposed to mediate between genotype and phenotype. Just as the cell (and not its genome) functions as the unit of organic structure and function, so the morphogenetic field (and not the genes or the cells) is seen as a major unit of ontogeny whose changes bring about changes in evolution.

An argument is proposed to explain the origin of large metazoans, based on the regulatory processes that underlie the morphogenetic organization of pattern in modern animals. Genetic regulatory systems similar to those used in modern, indirectly developing marine invertebrates are considered to indicate the Precambrian regulatory platform on which were erected innovations that underlie the development of macroscopic body plans. Those systems are genetic regulatory programs that produce groups of unspecified "set-aside cells" and hierarchical regulatory programs that initially define regions of morphogenetic space in terms of domains of transcription factor expression. These ideas affect interpretation of the development of arthropods and chordates as well as interpretation of the role of the genes of the homeotic complex in embryogenesis.

There has been a resurgence of interest in comparative embryology. It is now important to be able to compare gene expression in different species at similar developmental stages. One phenomenon which may make it difficult to compare embryos in this way is heterochrony--a change in developmental timing during evolution. It is not clear whether heterochrony can affect the intermediate stages of embryonic development, when many important genes involved in pattern formation are expressed. A prevalent view is that these so-called phylotypic stages are resistant to evolutionary change because they are when the body plan is laid down. Haeckel's famous drawings, which show different vertebrates developing from virtually identical somite-stage embryos, are still used to support this idea. I have reexamined the morphological data relating to developmental timing in somite-stage embryos. The data reveal striking patterns of heterochrony during vertebrate evolution. These shifts in developmental timing have strongly affected the phylotypic stage, which is therefore poorly conserved and is more appropriately described as the phylotypic period. This is contrary to the impression created by Haeckel's drawings, which I show to be inaccurate and misleading. The study of gene expression in embryos which show heterochrony could give important insights into evolutionary and developmental mechanisms.