Hemichordates and the origin of chordates John Gerhart1, Christopher Lowe2 and Marc Kirschner3 Hemichordates, the phylum of bilateral animals most Hemichordates should offer the best opportunity to dis- closely related to chordates, could reveal the evolutionary cern the evolutionary origins of these traits. However, origins of chordate traits such as the nerve cord, notochord, beyond their gill slits, they bear little resemblance to gill slits and tail. The anteroposterior maps of gene chordates [1,2,3]. The phylum contains two classes: expression domains for 38 genes of chordate neural enteropneusts (‘acorn worms’) and pterobranchs. Enter- patterning are highly similar for hemichordates and opneusts are worm-like, solitary animals, a few centi- chordates, even though hemichordates have a diffuse metres to two metres in length, with up to several nerve-net. About 40% of the domains are not present in hundred pairs of gill slits. They dwell in burrows or under protostome maps. We propose that this map, the gill slits objects in intertidal zones worldwide. The body has three and the tail date to the deuterostome ancestor. The map parts (prosome, mesosome and metasome), each with a of dorsoventral expression domains, centered on a coelomic cavity or paired cavities, whereas chordates have Bmp–Chordin axis, differs between the two groups; but one coelom pair. The prosome is the proboscis, the hemichordates resemble protostomes more than they do mesosome is the collar, and the metasome contains the chordates. The dorsoventral axis might have undergone pharynx, gonads and gut (Figure 1). Enteropneusts bur- extensive modification in the chordate line, including row with the muscular proboscis, and move within the centralization of the nervous system, segregation of burrow by the action of cilia and muscles of the body wall. epidermis, derivation of the notochord, and an inversion of The mouth is positioned ventrally, between the prosome organization. and the mesosome. As suspension and detritus feeders, they sweep particles into the mouth by cilia, or ingest Addresses sand coated with organic materials. Of the 70 hemichor- 1 Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3200, USA date species, some develop directly from an egg to a 2 Department of Organismal Biology and Anatomy, 1027 East 57th juvenile, and others develop indirectly, with a planktonic Street, University of Chicago, Chicago, IL 60637, USA tornaria larva as an intermediate. Pterobranchs, the other 3 Department of Systems Biology, Harvard Medical School, Boston, class, are minute (1mm), sessile, stalked, deep-ocean MA 02115, USA animals that live in colonies. They too have a three-part Corresponding author: Gerhart, John ([email protected]) body, but only one pair of gill slits, or none. Ciliated tentacles of the mesosome pass food particles to the mouth. All 10 or so species are direct developers. Current Opinion in Genetics & Development 2005, 15:461–467 This review comes from a themed issue on In the 1880s, William Bateson [4,5,6] first compared Pattern formation and developmental mechanisms hemichordate and chordate anatomy. Studying the Edited by William McGinnis and Cheryll Tickle direct-developing enteropneust Saccoglossus kowalevskii, he perceived major chordate traits and placed hemichor- Available online 17th June 2005 dates in the chordate phylum. To him, a short, stiff rod of 0959-437X/$ – see front matter cells, projecting from the anterior gut into the proboscis, # 2005 Elsevier Ltd. All rights reserved. was a notochord (see ‘stomochord’ in Figure 1). Nerves of the dorsal midline looked like a dorsal hollow nerve cord of DOI 10.1016/j.gde.2005.06.004 a centralized nervous system. Gill slits were obviously present, and he judged them to resemble those of amphioxus. Although Bateson didn’t dwell on it, Bur- Introduction don-Jones [7] later examined the post-anal tail of the The notochord, dorsal hollow nerve cord, gill slits and a juvenile and found it to resemble the chordate tail. Bateson post-anal tail are phylotypic traits of chordates. Less and, later, Goodrich [8] saw a possible pituitary homolog prominent are the endostyle/thyroid, the pituitary, left– in the proboscis pore region of hemichordates and a pos- right asymmetries, and the inverse dorsoventral organiza- sible homolog of the endostyle/thyroid in the pharynx. tion of chordates relative to that of protostomes. In chordate development, Spemann’s organizer is distinc- However, by the 1940s, biologists became skeptical of tive not only as a key signaling center of the chordate homologies, except for gill slits, and hemichordates were gastrula but also as the precursor of the notochord, gill slit relegated to a phylum of ‘half chordates’ [1,2]. Their endoderm, and prechordal endomesoderm. Did these development was largely unstudied for 50 years, with a originate entirely within the chordate lineage or were few exceptions [9,10,11]. In this review, we focus on some already present in non-chordate ancestors? recent comparisons of hemichordates and chordates www.sciencedirect.com Current Opinion in Genetics & Development 2005, 15:461–467 462 Pattern formation and developmental mechanisms Figure 1 (a) (b) (c) Proboscis Collar Proboscis Gill Collar slit Heart Mouth Kidney Pharynx Tail Gut Stomochord Anus Mouth Saccoglossus kowalevskii, a direct-developing enteropneust hemichordate of the US Atlantic coast. (a) Adult female. Note the white proboscis, orange collar, tan pharynx and gut, and grey ovaries. Length: 10–18 cm. (b) Juvenile, a week after hatching, two weeks after fertilization of the egg. Length: 1 mm (c) The ‘notochord’, so-called by Bateson (see text), now called the stomochord, located between the proboscis and collar. Shown in sagittal section. Redrawn from Bateson [5]. regarding their gene sequences and expression domains. pterobranch-like adult. Rows of cilia, within a diffuse We discuss the updated deductions about their common nervous system, moved dorsally by a series of ancestor and, hence, about the origin of chordates. evolutionary intermediates, and eventually interna- lized at the midline as a new, centralized, dorsal nerve- Modern phylogenies cord. From the sessile adult, gill slits, a notochord, and Recent DNA phylogenies place hemichordates as the sexual maturity were transferred to the larva by sister group of echinoderms [12–14]. Together, these neoteny, forming a motile protochordate adult. two are the sister group of chordates (Figure 2). The 3. Bilaterial ancestor hypothesis: in the 1990s, chordates three phyla constitute the supertaxon of deuterostomes (mice, frogs and fish) were found to share many (Xenoturbella might be a fourth [15]). The lineage from domains of gene expression with protostomes (mainly the ancestor of deuterostomes to the ancestor of chordates Drosophila), such as Hox domains in the posterior head bore no branches to extant groups. Paleontology of the and trunk; emx and otx domains in the anterior head; past decade has uncovered a profusion of Cambrian pax6 and six expression in light receptive organs of the deuterostomes (e.g. vetulicolians, yunnanozoans) that head; many genes of neuron identity and differentia- has still to be reconciled with this simple phylogeny [16]. tion; nkx2.5 in the heart; and hh/bmp in the gut and visceral mesoderm [19,20]. All these domains were Other bilateral animals, comprising approximately 25 ascribed to the ancestor of bilateral animals. Given the phyla, are protostomes. The last common ancestor of existence of such a complex ancestor, the evolution of deuterostomes and protostomes is the ancestor of all deuterostomes and chordates entailed less innovation bilateral animals, one node before the deuterostome than was previously thought. ancestor. 4. Inversion hypothesis [21,22]: the chordate ancestor had a protostome-like arrangement of organs in the Four venerable hypotheses of chordate dorsoventral dimension: a ventral centralized nervous origins system, ventral musculature and a dorsal heart. A Consistent with the modern phylogeny are four hypoth- descendent in the chordate line inverted its body eses for the origin of chordates from a deuterostome dorsoventrally and evolved a mouth on the new ventral ancestor. We present these and comment on them in surface, making chordate anatomy the inverse to that light of recent results. of protostomes. As recent support, bmp was found to be expressed dorsally in protostome embryos but ven- 1. Hemichordate hypothesis: for Bateson [17], chordates trally in chordate embryos, whereas expression of evolved by the exaggeration of structures of a chordin, which encodes a Bmp antagonist, is the hemichordate-like ancestor that had a dorsal central reverse. This Bmp–Chordin axis, which underlies nervous system. Goodrich [8] proposed that the two dorsoventral patterning in all bilateral animals, is anterior coelom pairs shrank to preotic somites in inversely oriented. Motoneurons and interneurons chordates, and dorsal anterior structures were dis- develop in the Bmp-free ectoderm, and sensory placed around the front end to ventral locations. neurons develop in the Bmp area. Although not 2. Auricularian hypothesis: for Garstang [18], the chor- logically required, the hypothesis usually starts with an date ancestor was a motile, ciliated larva of a sessile, ancestor having a centralized nervous system. Hemi- Current Opinion in Genetics & Development 2005, 15:461–467 www.sciencedirect.com Hemichordates and the origin of chordates