development of radial and biradial symmetry: The evolution of bilaterality, The

American Zoologist, Sep 1998 by Martindale, Mark Q, Henry, Jonathan Q

The Development of Radial and Biradial Symmetry: The Evolution of Bilaterality'

MARK Q. MARTINDALE2 AND JONATHAN Q. HENRY

SYNOPSIS. Understanding the evolutionary origin of novel metazoan body plans continues to be one of the most sought after answers in biology. Perhaps the most profound change that may have occurred in the Metazoa is the appearance of bilaterally symmetrical forms from a presumably radially symmetrical ancestor. The symmetry properties of bilaterally symmetrical larval and adult metazoans are generally set up during the cleavage period while most "radially" symmetrical cnidarians do not display a stereotyped cleavage program. Ctenophores display biradial symmetry and may represent one intermediate form in the transition to bilateral symmetry. The early development of cnidarians and ctenophores is compared with respect to the timing and mechanisms of axial determination. The origin of the dorsal-ventral axis, and indeed the relationships of the major longitudinal axes, in cnidarians, ctenophores, and bilaterian animals are far from certain. The realization that many of the molecular mechanisms of axial determination are conserved throughout the Bilateria allows one to formulate a set of predictions as to their possible role in the origins of bilaterian ancestors.

INTRODUCTION

Recent reports indicate that there is surprising conservation in the cellular and molecular basis of embryonic patterning events in organisms as diverse as mice and insects. One can only wonder how deeply rooted these mechanisms are within the Metazoa, and how such a diverse array of creatures could have evolved from an ancestor that utilized these conserved patterning mechanisms. Bilaterally symmetrical organisms, the Bilateria, are likely to have evolved from some kind of ancestor with a cnidarian- or ctenophore-like level of body construction, as members of the so-called "Radiata" (Morris, 1993; Wainright et al., 1993; Brusca and Brusca, 1990). When attempting to formulate theories about how such a radical change in the body plan could arise, one must have some understanding of the developmental basis for their construction. In contrast to many bilaterians, we know little about the development and evolution of members of the Radiata. The evolution of the Bilateria, by definition, is ultimately concerned with the origins of the dorsal-ventral and bilateral axes, yet little information is currently available to suggest how these major body axes might have evolved. This paper reviews various aspects of axial specification in the Radiata, including some of recent work on ctenophore embryos, and addresses issues regarding the invention of stereotypical cleavage programs and the possible transitions between radial, biradial and bilaterally symmetrical body plans.

THE RADIATA

The two eumetazoan phyla which comprise the Radiata are the cnidarians and the ctenophores. The major adult body axis of both ctenophores and cnidarians is the "oral-aboral" axis. In both phyla, the outer epidermal epithelium surrounds an inner gastrodermic pouch that opens at the mouth (Fig. 1). Separating these two layers is the mesoglea, a largely acellular extracellular matrix. Although individual cells reside within or wander through the mesoglea, no true mesodermal tissue layer is present, and hence these organisms are often referred to as "diploblastic." While the gastric cavity is blind in cnidarians, ctenophores possess two small openings on either side of the apical organ, the anal pores, which connect the gut cavity to the outside environment. Effectively, the mouth also acts as an anus, since the anal pores are too small to pass the majority of undigested matter

Due to the complex and diverse life history strategies present in the Cnidaria, distinctly different benthic and pelagic forms are often generated. Most cnidarians display variations of one or both of the following morphs: a sessile polyp with a mouth surrounded by tentacles located at the oral end of the longitudinal axis and a basal disc or holdfast located at the aboral end (Fig. lA). Alternatively, a free-living pelagic medusa may be formed that possesses its mouth at the tip of the manubrium, which is suspended beneath a swimming bell (Fig. lB). In most cnidarians, embryogenesis results in a solid ciliated planula larva (with no mouth or functional gut) that has only a single recognizable, anterior-posterior, axis. The planula eventually metamorphoses into a sessile polyp in which the anterior pole of the planula (defined by swimming direction) becomes the basal disc (holdfast) and the posterior pole becomes the mouth. In hydrozoans, the polyp later buds a pelagic medusa which will go on to form functional gametes. In anthozoans, the polyp morph produces gametes directly. On the other hand, virtually all ctenophores are pelagic animals with direct development. There is no true larval phase and embryogenesis results in the production of a cydippid stage adult. In some orders, the cydippid undergoes additional growth that transforms it into a secondarily-derived adult, but this does not entail a radical metamorphosis or change in the basic body plan.