Hemichordata

Hemichordata is a pivotal marine phylum of Deuterostomia comprising ~130 living species divided into two morphologically contrasting classes: solitary, burrowing Enteropneusta (the acorn worms, such as Saccoglossus kowalevskii, Ptychodera flava, and Balanoglossus) and miniature, colonial, tube-building Pterobranchia (Rhabdopleura and Cephalodiscus, together with the vast Paleozoic fossil record of planktonic Graptolithina).

First united as the sister group to Echinodermata inside the clade Ambulacraria by Elias Metschnikoff in 1881 (who discovered that the planktonic tornaria larva of Indirect-developing acorn worms is nearly identical in ciliary band topology and hydrocoel development to the bipinnaria/auricularia larva of sea stars and sea cucumbers) and confirmed by every molecular and phylogenomic dataset (Bromham & Degnan, 1999; Simakov et al., 2015), Hemichordata holds a unique position in evolutionary biology: while echinoderms secondarily evolved pentaradial adult symmetry and lost pharyngeal gill slits, enteropneust acorn worms retain the ancestral bilateral, gill-slit-bearing body plan of the last common deuterostome ancestor (~550 Ma).

Both enteropneusts and pterobranchs share a tripartite (three-region) body plan (archimery), each housing its own coelomic compartment formed by enterocoely from the embryonic archenteron:

1. Protosome (Proboscis or Cephalic Shield — Unpaired Protocoel): A muscular, ciliated anterior organ used by acorn worms for peristaltic burrowing and mucus-ciliary deposit feeding (and by pterobranchs to secrete their collagenous coenecium tube). The single protocoel opens to the exterior via a dorsal left proboscis pore (homologous to the echinoderm hydropore/madreporite) and houses the heart–glomerulus complex—an excretory ultrafiltration organ driven by blood pressure across podocytes lining the stomochord.
2. Mesosome (Collar — Paired Mesocoels): A cylindrical collar surrounding the ventral mouth. Extending forward from the dorsal roof of the buccal cavity into the base of the proboscis is a hollow, vacuolated endodermal diverticulum called the stomochord. Although William Bateson (1885) originally homologized the stomochord with the chordate notochord (coining the name Hemichordata, "half-chordate"), modern gene expression studies show that the stomochord does not express the canonical notochord transcription factor Brachyury or FoxA in a notochordal program and is instead an independent endodermal support rod for the heart–glomerulus complex. Dorsal to the gut inside the collar runs a hollow collar nerve cord (formed by neurulation-like ectodermal invagination in some species) continuous with a basiepidermal nerve net.
3. Metasome (Trunk — Paired Metacoels): An elongate posterior trunk perforated dorsolaterally in enteropneusts by up to 100+ pairs of ciliated pharyngeal gill slits supported by acellular collagenous gill bars (secreted by endodermal cells, unlike the cellular neural-crest cartilage of vertebrates), followed by a straight digestive intestine and terminal anus.

For over a century, graptolites (Graptolithina)—colonial marine fossils preserved as carbonized sawblade impressions in black shales from the Middle Cambrian through the Early Carboniferous (~510–320 Ma) and prized by geologists as the premier index fossils for subdividing Ordovician and Silurian time—were an evolutionary enigma.

Beginning with Roman Kozłowski (1948) and confirmed via electron microscopy by Noel Dilly, Barrie Rickards, and Charles E. Mitchell, paleontologists proved that living pterobranchs of the genus Rhabdopleura are extant benthic graptolites:

• With its muscular cephalic shield (protosome), a Rhabdopleura zooid secretes its housing tube (theca) as a series of alternating left- and right-handed half-rings (fuselli) that meet in a diagnostic zigzag suture line, overlaid by an outer cortical layer of crossed collagen fibrils—matching the exact ultrastructure of Ordovician graptolite periderm.
• Paleozoic planktic graptolites (Graptoloidea) simply detached from the seafloor during the Tremadocian (Early Ordovician, ~485 Ma) to float in the open ocean as suspension-feeding phytoplankton grazers before going extinct, while their benthic encrusting cousins (Rhabdopleura) survived to the present day.

Although enteropneust acorn worms (Saccoglossus kowalevskii) lack a centralized brain or paired eyes inside their proboscis—possessing only a diffuse basiepidermal nerve plexus thickened at the proboscis base and collar—groundbreaking in situ hybridization studies by Christopher J. Lowe, Marc W. Kirschner, John Gerhart, and colleagues (2003, 2006) revealed that the surface ectoderm of Saccoglossus expresses the entire anteroposterior and dorsoventral transcription-factor map of the vertebrate forebrain, midbrain, and hindbrain in identical spatial register:

1. Anteroposterior Brain Zones Without a Brain: Going from the anterior tip of the proboscis backward across the collar and into the gill-slit trunk, Saccoglossus ectoderm expresses:
   • Anterior Proboscis (Vertebrate Telencephalon/Forebrain homolog): Six3, FoxG1 (BF-1), Rx, and Dlx;
   • Posterior Proboscis & Collar (Vertebrate Diencephalon & Midbrain homolog): Otx, Pax6, and Lim1/Lhx1;
   • Collar–Trunk Boundary (Vertebrate Midbrain–Hindbrain Isthmic Organizer / MHB homolog): A sharp juxtaposition of Otx and Gbx overlapped by concentric rings of Fgf8/17/18, Wnt1, and Engrailed (En);
   • Pharyngeal Trunk (Vertebrate Hindbrain & Spinal Cord homolog): Collinear Hox genes (Hox1, Hox3, Hox4, Hox5... Hox11/13).
2. Pharyngeal Gill Slits (Pax1/9–Six1–Eya–FoxI): Comparative genomics of Saccoglossus kowalevskii and Ptychodera flava (Simakov et al., 2015) further identified a conserved deuterostome pharyngeal gene cluster (Pax1/9–Slc25a21–Mipol1–FoxA) that patterns the endodermal gill slits of both acorn worms and vertebrates—proving that the last common ancestor of Ambulacraria and Chordata already possessed ciliated pharyngeal gill slits and the complete molecular blueprint of the vertebrate central nervous system before centralized brain condensation evolved.

Why did echinoderms and hemichordates diverge so dramatically in adult body plan if they are sister phyla (Ambulacraria)?

Although adult sea stars (pentaradial, calcitic stereom endoskeleton, water vascular system, no gill slits) and adult acorn worms (bilateral, soft-bodied burrowers with 100+ gill slits) look completely unalike, early Paleozoic fossils bridge the gap: Cambrian stylophoran ("calcichordate") and cinctan stem-echinoderms (Cothurnocystis, Gyrocystis) were asymmetric/bilateral animals that possessed pharyngeal gill slits perforated through a calcitic theca! Conversely, the Burgess Shale fossil Spartobranchus tenuis (Caron et al., 2013) shows that 508-million-year-old enteropneust worms lived inside fibrous branching tubes virtually identical to those of pterobranchs, demonstrating how solitary burrowing enteropneusts and colonial tentaculate pterobranchs diverged from a tube-dwelling ambulacrarian ancestor.

How does BMP/Chordin dorsoventral signaling in Saccoglossus compare to vertebrates and arthropods?

As demonstrated by Christopher Lowe and colleagues (2006), Saccoglossus expresses BMP2/4 along its dorsal midline and the BMP antagonist Chordin on its ventral (mouth) side—matching the orientation of protostomes (Drosophila) rather than vertebrates (which inverted their dorsoventral axis so that BMP4 is ventral and Chordin/notochord is dorsal). Notably, in Saccoglossus, high BMP signaling does not repress neural differentiation as it does in vertebrates and insects; instead, the basiepidermal nerve net differentiates across both high-BMP dorsal and high-Chordin ventral ectoderm.

1. Lowe, C. J., Wu, M., Salic, A., Evans, L., Lander, E., Stange-Thomann, N., ... & Gerhart, J. (2003). Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell, 113(7), 853–865. doi:10.1016/S0092-8674(03)00469-000469-0)
2. Simakov, O., Kawashima, T., Marlétaz, F., Jenkins, J., Koyanagi, R., Mitros, T., ... & Gerhart, J. (2015). Hemichordate genomes and deuterostome origins. Nature, 527(7579), 459–465. doi:10.1038/nature16150
3. Caron, J. B., Conway Morris, S., & Cameron, C. B. (2013). Tubicolous enteropneusts from the Cambrian period. Nature, 495(7442), 503–506. doi:10.1038/nature12017
4. Mitchell, C. E., Melchin, M. J., Cameron, C. B., & Maletz, J. (2013). Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia, 46(1), 34–56. doi:10.1111/j.1502-3931.2012.00319.x