Evolution and Development of the Chordates: Collagen and Pharyngeal Cartilage

Abstract

Chordates evolved a unique body plan within deuterostomes and are considered to share five morphological characters, a muscular postanal tail, a notochord, a dorsal neural tube, an endostyle, and pharyngeal gill slits. The phylum Chordata typically includes three subphyla, Cephalochordata, Vertebrata, and Tunicata, the last showing a chordate body plan only as a larva. Hemichordates, in contrast, have pharyngeal gill slits, an endostyle, and a postanal tail but appear to lack a notochord and dorsal neural tube. Because hemichordates are the sister group of echinoderms, the morphological features shared with the chordates must have been present in the deuterostome ancestor. No extant echinoderms share any of the chordate features, so presumably they have lost these structures evolutionarily. We review the development of chordate characters in hemichordates and present new data characterizing the pharyngeal gill slits and their cartilaginous gill bars. We show that hemichordate gill bars contain collagen and proteoglycans but are acellular. Hemichordates and cephalochordates, or lancelets, show strong similarities in their gill bars, suggesting that an acellular cartilage may have preceded cellular cartilage in deuterostomes. Our evidence suggests that the deuterostome ancestor was a benthic worm with gill slits and acellular gill cartilages.

Development and evolution of chordate cartilage

“…We have presented evidence previously that gill slits in hemichordates, lancelets, and vertebrates are homologous (Rychel et al, 2006;Swalla, 2007) and that gill bars in hemichordates and cephalochordates are composed of a protein similar to vertebrate type II collagen (Rychel et al, 2006). Now we present new data that show that the pharyngeal endodermal cells in hemichordates and lancelets express a fibrillar collagen and the pharyngeal endoderm in hemichordates also expresses the invertebrate homolog to vertebrate Sox8/9/1O, SaxE.…”

“…Clones from both the triple helical domain and C terminal domain were used for in situ hybridization . The parsimony gene tree was constructed as previously reported (Rychel et al, 2006) and two new type II collagen sequences from lamprey were added to the dataset. Briefly, complete or partial amino acid sequences from the fibrillar collagen triple helical domains were aligned in Clustal X (Jeanmougin et al,'98).…”

“…1), and this tissue is secr eted by chondrocytes of neural crest origin (Noden, '78;Kimmel et a1., 2001 ). A major difference, how ever, is that vertebrate pharyngeal cartilage is a cellular tissue while the hemichordate and lancelet pharyngeal cartilages are acellular (Cole and Hall, 2004a;Rychel et al , 2006). Since lancelets and hemichordates lack chondrocytes in their pharyngeal cartilage, it is not obvious which cells are responsible for secreting the cartilage matrix.…”

“…Placodes and neural crest-like cells have not been described in hemichordates and are lacking in lancelets, even though tunicates clearly contain placodes and may have neural crest-like cells (Swalla, 2007 for review). Yet both hemichordates and lancelets have fibrillar collagen in their pharyngeal cartilages as seen by transmission electron microscope (TEM) and immunohistochemistry (Rahr, '82;Pardos and Benito, '88;Rychel et al, 2006), even though the gill bar cartilages are acellular (Cole and Hall, 2004b;Rychel et al, 2006).…”

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).…”