Integrating Cellular and Molecular Approchaes into Studies of Development and Evolution: The Issue of Morphological Homology

Understanding the development and evolution of complex morphological characters requires broad, multidisciplinary approaches. By combining biological imaging, phylogenetic analyses, embryological manipulations and additional modem molecular techniques (e.g., whole mount in situ hybridization), we can address fundamental questions, such as the determination of homology. Many of the novel structures that evolved in vertebrates and distinguish them from their ancestors (such as jaws and the mechanosensory lateral line) are derived embryonically from two migratory ectodermal tissues, neural crest and/or various epidermal placodes. In particular, time-lapse cinematography of fluorescently labeled cells in living Xenopus and fish embryos has proved a powerful technique, revealing new information on migration and differentiation. These data allow us to reexamine the developmental criterion for morphological homology. There are three criteria for determining morphological homology of a structure between species: position (anatomical location), development (common origin, gene expression and/or cell behavior), and phylogeny (identification of the structure in an outgroup). Currently the phylogenetic criterion is the most regularly employed. Previous problems with the application of the developmental criterion were based on a paucity of detailed comparative developmental data and the overlooked assumption that ontogenies can not change during evolution and remain homologous while morphologies can. Homology has been defined as similarity due to continuity of information. The rejection of developmental data as a homology criterion is based on emphasizing lack of similarity without considering the information on continuity provided by these data. Often missing from previous analyses are the concepts of multiple developmental mechanisms in the formation of a structure (including such issues as developmental redundancies) and that ontogenies can change during evolution. By including these two concepts in a broadly comparative analysis, such problems as seemingly different developmental and genetic bases for homologous structures, can be explained and are even expected. As examples of how such an analysis can be done, we compared the development of the neural tube and lateral line among several vertebrate species. We show that while across species a given structure\u27s ontogeny may differ, a more broadly comparative developmental criterion using modern cell and molecular biological techniques provides a good homology criterion. Also, we find that molecular homology alone is not yet a good basis for morphological homology. While we would argue that a phylogenetic perspective is important (and critical for polarizing evolutionary changes), it is not essential for our usage of the developmental criterion. Thus, a broadly comparative and detailed understanding of developmental mechanisms makes for a robust criterion of homology