656 Heredity (2006) 97, 23~-243 ~ 2006Nature Publishing Group Allrigh ts reserved 0018·067X/06 530.00 www.nature.com/hdy SHORT REVIEW • Building divergent body plans with similar genetic pathways BJ Swallau 3 'Center for Developmental Biology, Department of Biology, University of Wa shington, Seattle, WA 98195-1800, USA;' Friday Harbor Laboratories, University of Washingtoll, Friday Harbor, WA 98250-9299, USA; "Smithsonian Marine Station , 701 Seaway Drive, Fort Pierce, FL 34949-3140, llSA Deuterostome animals exhibit widely divergent body plans. second way of evolving a divergent body plan is to become Echinoderms have either radial or bilateral symmetry, colonial, as seen in hemichordates and tunicates. Early hemichordates include bilateral enteropneust worms and embryonic development and gastrulation are similar in all colonial pterobranchs, and chordates possess a defined deuterostomes, but, in chordates, the anterior-posterior dorsal-ventral axis imposed on their anterior-posterior axis. axis is established at right angles to the animal-vegetal Tunicates are chordates only as larvae, following meta­ axis, in contrast to hemichordates and indirect-developing morphosis the adults acquire a body plan unique for the echinoderms. Hox gene sequences and anterior-posterior deuterostomes. This paper examines larval and adult body expression patterns illuminate deuterostome phylogenetic plans in the deuterostomes and discusses two distinct ways relationships and the evolution of unique adult body plans of evolving divergent body plans. First, echinoderms and within monophyletic groups. Many genes that are considered hemichordates have similar feeding larvae, but build a new vertebrate 'mesodermal' genes, such as nodal and brachyury adult body within or around their larvae. In hemichordates T, are likely to ancestrally have been involved in the and many direct-developing echinoderms, the adult is built formation of the mouth and anus, and later were evolutiona­ onto the larva, with the larval axes becoming the adult axes rily co-opted into mesoderm during vertebrate development. and the larval mouth becoming the adult mouth. In contrast, Heredity (2006) 97, 235-243. doi:10.1038/sj.hdy.6800872; indirect-developing echinoderms undergo radical metamor­ published online 26 July 2006 phosis where adult axes are not the same as larval axes. A Keywords: chordate evolution; body plans; coloniality; tunicates; hemichordates; evolution and development Deuterostome phylogenetic relationships 2005; Rychel et al, 2006). There is both molecular and morphological evidence that the Ambulacraria are Deuterostome phylogenetic relationships have been monophyletic (Cameron et al, 2000; Peterson, 2004; Smith reviewed extensively elsewhere (Schaeffer, 1987; Camer­ et al, 2004). Similarities in the larvae of echinoderms and on et ai, 2000; Bourlat et al, 2003; Smith et al, 2004; Blair hemichordates have been noted for years (Figure 2; and Hedges, 2005; Zeng and Swalla, 2005; Delsuc et al, Morgan, 1891; Dautov and Nezlin, 1992; Strathmann and 2006) so will be briefl y discussed here. Deuterostomes Eernisse, 1994; Nielsen, 1997) and echinoderms and are monophyletic, and include two great clades: Ambu­ hemichordates have recently been shown to share motifs lacraria, which consists of Echinodermata and Hemi­ in three posterior Hox genes, Hox 11 /13a, 11/13b and 11/ chordata (Figure 11; Cameron ei al, 2000; Peterson, 2004; Be, as discussed later (Peterson, 2004). This raises the Smith et al, 2004), and Chordata, which consists of interesting question of how the two phyla have such Tunicata, Cephalochordata (Iancelets), and Vertebrata different adult body plans, when they have such similar (Figure 1II; Cameron ei al, 2000; Zeng and Swalla, 2005). larvae. Xenoturbellida, a potentially new phylum of the Deuter­ Conversely, within chordates, Tunicata is the only ostomia that has been described, is thought to be related subphylum that is classified by larval, rather than adult to the Ambulacraria, but the exact placement within the characteristics (Zeng and Swalla, 2005). Tunicates are deuterostomes is not yet clear (Bourlat et al, 2003). monophyletic (Swalla et al, 2000) and have a unique There is a plethora of evidence for echinoderms and adult body plan, including the cellulose tunic, as hemichordates as sister groups (Peterson, 2004; Smith discussed in Zeng and Swalla (2005). It is difficult to et al, 2004; Zeng and Swalla, 2005), so features that place tunicates reliably within the deuterostomes, due to hemichordates share with chordates were likely to have the long branches found for most of their genes (Winchell been present in the deuterostome ancestor (Gerhart et al, et al, 2002; Blair and Hedges, 2005; Zeng and Swalla, 200?). Interestingly, new genome anal yses suggest that Correspondence: 81 Siualla, Department of Biology, University of tunicates are more related to vertebrates than cephalo­ Wasilmgton, Box 351800, 24 Kincaid Hall, Seattle, WA 98195, USA. chordates, but these results could be an artifact of E-mait: bJ [email protected] incomplete data from cephalochordates and hemichor­ Received 1 January 2006; accepted 2 June 2006; published online 26 dates (Blair and Hedges, 2005; Philippe 2005; Delsuc July 2006 et al, et al, 2006). Understanding the position of the tunicates Evolution of divergent body plans BJ Swalla 236 m Crino idea r o :x Asteroidea fr Z o Ophiuroidea c 'It- m :Xl Holothuroidea ~ :s: ~ :J> Echinoidea l'; :x Harr iman iidae ~ :s:m n :x Pterobranchia o :Xl ~ Ptychoderidae ~ ~ L.... Xenoturbellida Appendicularia "­ Phlebobranchia -i c: Thaliacea @ . z -- Aplousobranchia \ '. ~ Stolidobranchia II Figure 2 Deut erostome larvae, showing (a) a sea star echinode rm Molgulidae lar vae. (b) a hem ichordate tornaria larva and (c ) a tunicate larva, all oriented with the mouth to the left and anus to the bott om . (a) Sea star larvae have on anterior (top left), which was the original an imo! Cephalochordata «x: - ft' ,·-=-- po le of the egg. (b) Anterior in the hernichordate tornaria larva is the ap ical tuft (top of ph oto). (a, b) Both of these larvae feed with ciliary beating and have well-d evelop ed guts and coeloms . The L....__ Vertebrata mouth of the sea star and hem ichord are lar vae are seen to the left (arrow). The posterior anus forms at the former vegetal pole (arrows ~igur e 1 Curren t deuterostom e phylogeny, with the thr ee major at bottom ). In hem ichord ates, the lar val mouth becom es the ad ult invertebrate clades mark ed on the right : Echinoderma ta, Hcrni­ m.outh and the proboscis develops anterior to the mouth. The gill chorda ta and Tunicata . Vert ebrates and Cephalochorda ta (lancelets) slits and abdomen of the worm w ill develop posteriorly. (c ) The form a fourth clade,Chordata. Ciliated Amb ulacraria lar vae (I) and tu.nicate larva is nonfeed ing an d lacks a heart, blood and gu t, which Tunicata tadpole larvae (II) are likely to hav e separa te origi ns. will develop after metam orphosis. An arrow marks the anterior, Uncer tainties in the Tunicata phylogeny ar e marked by dotted lines. wh ere the mouth will form after metamorphosis, but is not yet Mod ified from Zeng and Swalla (2005). open. There is no anus at this stage. within the deuterostomes will require continued phylo­ echinoderms and hemichordates share similar genetic genetic and genomic analyses, coupled with careful pathways during the em bryonic and larval stages stud ies of evolutionary and developmental processes, (Shoguchi ei al, 1999). In hemichordates and indirect­ including analyses of gene networks (Davidson and de veloping echinoderms, the animal-vegetal axis of the Erwin, 20(6). egg becomes the anterior-posterior axis of the larva, so a mouth is form ed secondar ily at the location where the archenteron contacts the ectode rm (Figures 2-4; Chea Early development in the deuterostomia et al, 2005). In contrast, in cho rdates, gastru lation results All d euterostomes gastru late at the vegetal pol e, thus the in the movement of large amounts of mesoderm into the blastopore is formed at or near the vegetal pole, later arche nteron, in ord er to form the notochord and the becoming the anus (Chea et ai, 2005). Ho wever, the su rround ing mu scular sornites, so the anterior-posterior chordate larvae of ascidians hav e completely different axis lies at a right an gle to the animal-vegetal axis (Chea structu res and functions than the larvae of echinoderms et ai, 2005). and hemichordates (Figure 2; Ettensohn et al, 2004). Man y echinoderm and hemichord ate species hav e feeding larvae that capture food by ciliary moti on and Different adult body plans built from can spend months feeding in the plankton (Figure 2; similar larvae Dautov and Nezlin, 1992; Strathmann and Eerni sse, 1994; Nielsen, 1997). On the other hand, chordate ascid ian Hemichordate tornaria larvae are similar morphologi­ larvae are nonfeeding, and mu st metamorphose in orde r cally to the bip innaria larvae of sea stars and the to be able to feed (Figure 2; Davidson et al, 2004). We auricularia larvae of sea cucumbers (Figures 2-4; Dautov believe that these larvae have independent evolutionary and Nezlin, 1992; Strathrnann and Eemisse, 1994; Urata origins (Zeng and Swalla, 2005). Ascidian embryos and and Yamaguchi, 2004). This type of larva, with a distinct larvae share many genetic pathways with chordate gut and three coeloms has been called collectively a embryos (Passamaneck and Di Gregario, 2005), while dipleurulid larva (Nielsen, 1997). Development of a Heredity Evolution ofdivergent body plans BJ Swalla 237 becomes the adult mouth of the worm, located in the collar region, while the posterior of the enteropneust worm is elaborated by growth posterior to the neck region (Urata and Yamaguchi, 2004). In summary, in enteropneust hemichordates, the adult body plan is dramatically different inmorphology from the larval body plan, but the adult retains the same anterior­ posterior and oral-aboral axes. In contrast, indirect-developing echinoderms exhibit a radical metamorphosis, where the axes of the adult body Figure 3 Echinoid development (a).