Development and evolution of chordate cartilage

Abstract

Deuterostomes are a monophyletic group of an imals con tai ni n g vertebrates, lancelets, tunicates, hemichordates, ech inoderms, and xenoturbellids. F our out of these six extant groups-vertebrates, la ncelets, tunicates, and h emichordates-have pharyngeal gill slits. All groups of deuterostome an im als that have pharyngeal gill slit s also have a pharyn geal sk eleton supporting the pharyngeal ope nin gs, except tunicates. We previously found that pharyngeal cartilage in hemichordates and ceph aloch ordat es contains a fibrillar collagen protein similar to vertebrate type II collagen, but unlike vertebrate cartilage, the in vertebrate deuterostome cartilages ar e acellular. We found SaxE and fibrillar collagen expression in the pharyngeal endodermal cells adjacen t to where the cartilages form . These same endodermal epithelial cells also express Pax.l /9 , a marker of pharyngeal endoderm in vertebrates, lancelets, tunicates, and hemichordates. In situ exp eriments with a cephalochordate fibrillar collagen al so showed expression in pharyn geal en dode rm, as well as the ectoderm a nd the mesodermal coelomic pou ches lining the gill bars. These results indicate that the pharyngeal en doderm al cells are re sp on sible for secr etion of the cartilage in hemichordates, wherea s in lancelets, all the pharyngeal cells su r r ou n din g the gill bars, ect odermal, endodermal, and mesodermal may be resp onsible for cartilage formation . We propose that endoderm secretion was primarily the ancestral mode of making pharyngeal cartilages in deutero stomes. Later the evolu ti on ary origin of neural crest allow ed co-opti on of the gene n etwork for th e secretion of pharyngeal cartilage matrix in the new migratory n eural cr est cell populations found in vertebrat es.

Col2-Cre recombinase is co-expressed with endogenous type II collagen in embryonic renal epithelium and drives development of polycystic kidney disease following inactivation of ciliary genes

“…Studies in chordates suggest that secretion of a fibrillar collagen with properties similar to the vertebrate type II collagen by endodermal epithelium was the ancestral mode of making pharyngeal cartilages, the gill bars supporting pharyngeal gill slits. The morphological similarity of these cartilage-like structures to hypertrophied basal laminae has also been discussed in several reports (Benito and Pardos, 1997;Rychel et al, 2006;Rychel and Swalla, 2007).…”

Man is but a worm: Chordate origins

“…Hypotheses discussed in this article are based on the understanding that hemichordates are the sister group to echinoderms, but echinoderms have highly derived adult body plans that share few homologies with chordates (Swalla, 2006). We have shown that hemichordates and lancelets share homologies that are not present in echinoderms or tunicates, such as unusual acellular pharyngeal cartilages (Rychel and Swalla, 2007). Consequently, morphological characters shared between hemichordates and chordates are likely to have been present in the deuterostome ancestor (Swalla and Smith, 2008).…”

Molecular genetic insights into deuterostome evolution from the direct-developing hemichordateSaccoglossus kowalevskii

“…Most of these are now rather weakly supported by both morphological and molecular datasets (Peterson et al 1999;Nieuwenhuys 2002;Lowe et al 2003Lowe et al , 2006Ruppert 2005). However, only gill slits, as primary ciliated pouches, may represent an ancestral feature of the deuterostomes (Ogasawara et al 1999;Okai et al 2000;Tagawa et al 2001;Cameron 2002;Rychel et al 2006;Rychel & Swalla 2007) and possibly the post-anal tail (Lowe et al 2003). A much more in depth discussion of hemichordate and chordate potential morphological homologies is discussed in Ruppert (2005).…”