Evolution in developmental biology: Of morphology and molecules

Abstract

Experimental embryologists, molecular biologists, evolutionary morphologists, paleontologists and most other modem practitioners of developmental biology met recendy (British Sodety for Developmental Biology Spring Meeting, Edinburgh, UK; organized by M. Akam, P. Holland and G. Wray) to discuss the evolution of development. Despite its broad purview, four unifying themes emerged from the meeting. First, similarities in molecular pathways in diverse organisms are revealing previously unappreciated levels of homology: the animals we study now seem more similar than we could possibly have anticipated. Second, comparisons of genetic pathways are leading to reevaluation of evolutionary relationships at all taxonomic levels. Third, the identification of patterns of variance and invariance at the levels of genome structure and gene expression are providing interesting insights into the evolution of developmental mechanisms. Finally, and perhaps most sisniflcanfly, data from a range of approaches from the paleontological through the morphological to the molecular are being integrated to give more complete images in a common biological language. Comparisons of gene expression patterns (primarily of the homeotic genes and gene encoding intercellular signalling molecules) are prompting reassessment of the relationships between body parts across members of different phyla. Structures which by morphological or paleontological criteria have not previously been considered homologous may in fact be related by common descent. Recent dam suggest that segmental (memmeric) boundaries along the body axis, as well as the limbs, gut, eyes and heart, and specification of muscle groups, may all be homologized from vertebrates to insects to nematodes. In general, these are regulatory homologies, reflecting common control mechanisms, and are not necessarily manifested in morphological details. Homeotic genes are thought to specify relative positions along an axis. Although they may define boundaries of specific structures within a phylum, these structural boundaries are not generally considered to be maintained between phyla. However, data presented by C. Tabin (Boston, USA) suggest that some boundaries defined by Hox genes in vertebrates may indeed be conserved in insects. The anterior boundaries of expression of particular Hox paralog groups in the mesoderm of mouse and chicken correlate with transitions between vertebral types; for example, the genes of paralog group 6 are expressed at the cervical-thoracic border, while group 9 genes are expressed at the thoracic-abdominal border. Expression of these genes therefore correlates with vertebral identity, rather than absolute or relative positions in the embryo. Conservation of these transitions appears to extend to the type of segment specified by the insect homologs of these genes; for example, the Drosopbaa homologs of vertebrate paralog groups 6-8 and 9.-13 are also expressed within the same segment types, Thus the body plan of the common ancestor of insects and vertebrates may have been divided into large-scale morphological units, retained in these animals today. Other body parts of vertebrates and insects may also be homologous at this regulatory level. In the Drosophila alimentary canal, the homeotic genes, which ate expressed primarily along the anteroposterior axis of the visceral mesoderm, control the position of gut constrictions via intercellular signalling molecules such as dpp. Transcription of these signalling molecules is under positive and negative control by the homeotic genes, which also regulate one another, either direcdy or throush growth factor intermediaries (M. Scott, Palo Alto). Intriguingly, Hox genes, as well as Bmpi (a homolog of