Cellular and molecular mechanisms of segmentation in annelids Steven M. Irvine and Mark Q. Martindale * The annelids are a diverse phylum of metamerically segmen ted animals. T hey are of special in terest embryologically because of their highly stereotyped pattern of development, much of which is shared by other spiralian phyla. They are also of interest phylogenetically for what they can tell us about the evolution of segmentation, and the relationships of coelomate protostomes in general. In this paper we review the embryology of the different annelid groups, showing considerable conservation of the basic character of segmentation, with modifications associated with evolving life history strategies. We also describe the current knowledge of molecular mechanisms of segmentation in annelids. The most is known at a cellular and molecular level about the phylogenetically derived leeches, while information is just emerging on the more basal annelids, the polychaetes and oligochaetes. This review is intended to provide a framework for comparison of the different annelid groups, and to suggest avenues for future research that might help to illuminate the evolution of annelid developmental patterns. Key words: Annelida / embryology / segmentation ©1996 Academic Press Ltd THE ANNELIDS are a speciose segmented protosome phylum, with great diversity in morphology and ecology. Within this diversity, however (Figure 1) they share a remarkable degree of conservation of basic developmental patterns. This review will describe some of those conserved patterns, concentrating on the development of the segmented body, both at cellular and molecular levels, as well as pointing out the significant differences between annelid groups. We are defining segmentation as the presence of serially repeated anatomical units or metameres. In annelids the ‘basic segment’ is characterized by an annularized cross-section, with bilateral chaetae, nephridia, a ganglion of the ventral nerve cord, and a segmental complement of longitudinal, circumfer- ential, and oblique muscles surrounding an endo- dermal gut tube (Figure 2). The metameres are considered to be serially homologous, sharing a common developmental origin. Thus changes in morphology along the body axis, as are seen in some representatives of all segmented phyla, must involve evolution of subprograms within an overall devel- opmental scheme for the serial production of seg- ments. The most rostral and caudal portions of the body axis are generally regarded as non-segmental and have different origins and ontogenetic trajectories. The annelids have historically been regarded as the sister group of the arthropods, together forming the Articulata. This group is united largely by the pres- ence of serially homologous body segments arising by teloblastic growth. 1 An annelid-like creature has been widely viewed as the likely common ancestor of this clade. However, recent evidence has called this assessment into question. Cladistic analyses of both molecular 2-4 and a combination of embryological and morphological data 5 indicate that annelids are more closely related to molluscs than to arthropods. These studies imply that either shared characteristics of protostome segmentation arose independently, or that segmentation arose once and subsequently was lost in many of the protosome phyla. These questions are central to the understanding of the evolution of segmental development and of the Metazoa as a whole. Their resolution will depend in part on understanding annelid segmentation and its relation- ship to the modes of segmentation seen in arthropods. It is fairly certain that the Annelida is a monophy- letic taxon. 1 As will become apparent below, early developmental events are highly conserved through- out the phylum. The phylum consists of three classes; Polychaeta, Oligochaeta and Hirudinida. The Poly- chaeta is comprised of approximately 10,000 known From the Committee on Evolutionary Biology, University of Chicago, 1025 E. 57th Street, Culver Hall 402, Chicago, IL 60637, and *Department of Organismal Biology and Anatomy, Committees on Evolutionary Biology, Developmental Biology, and Neurobiology, University of Chicago, 1027 E. 57th Street, Chicago, IL 60637, USA seminars in CELL &DEVELOPMENTAL BIOLOGY, Vol 7, 1996: pp 593–604 ©1996 Academic Press Ltd 1084-9521/ 96/ 040593 +12 $18.00/ 0 593