Insights from Amphioxus into the Evolution of Vertebrate Cartilage

Abstract

Central to the story of vertebrate evolution is the origin of the vertebrate head, a problem difficult to approach using paleontology and comparative morphology due to a lack of unambiguous intermediate forms. Embryologically, much of the vertebrate head is derived from two ectodermal tissues, the neural crest and cranial placodes. Recent work in protochordates suggests the first chordates possessed migratory neural tube cells with some features of neural crest cells. However, it is unclear how and when these cells acquired the ability to form cellular cartilage, a cell type unique to vertebrates. It has been variously proposed that the neural crest acquired chondrogenic ability by recruiting proto-chondrogenic gene programs deployed in the neural tube, pharynx, and notochord. To test these hypotheses we examined the expression of 11 amphioxus orthologs of genes involved in neural crest chondrogenesis. Consistent with cellular cartilage as a vertebrate novelty, we find that no single amphioxus tissue co-expresses all or most of these genes. However, most are variously co-expressed in mesodermal derivatives. Our results suggest that neural crest-derived cartilage evolved by serial cooption of genes which functioned primitively in mesoderm.

Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head

“…However, C. savignyi gill slits form when neither FGF3 nor FGF8/17/18 transcripts are detectable in the endoderm, indicating that endodermal FGFs are unlikely to control pharyngeal segmentation in this species. By contrast, the invertebrate chordate amphioxus deploys both FGF8/17/18 and FGFA (a likely ortholog of FGF3) in patterns virtually identical to their vertebrate orthologs, with both genes displaying iterated expression in the pharyngeal endoderm during gill slit formation (Bertrand et al, 2011;Meulemans and Bronner-Fraser, 2007). Given the basal phylogenetic position of amphioxus, these observations support a deeply conserved role for endodermal FGFs in chordate pharyngeal segmentation.…”

“…FGF signals then work through FGFRs and fli/ets to activate dlx expression and specify chondrogenic fate (Das and Crump, 2012). In lamprey, Id expression is lost by cranial NCCs soon after they enter the pharynx, whereas Twist, Fli/Ets, Dlx and FGFR are upregulated (Bronner-Fraser et al, 2003;Meulemans and Bronner-Fraser, 2007;Neidert et al, 2001). FGFs are also needed during this period for expression of the cartilage specifier SoxE1, supporting the conservation of a zebrafish-type chondrogenic specification mechanism.…”

“…However, urochordates lack any collagen-based skeletal tissue resembling vertebrate cellular cartilage. By contrast, the basal chordate amphioxus possesses an acellular pharyngeal skeleton composed of chondroitin sulfate proteoglycans and fibrillar collagen (Azariah, 1973;Meulemans and Bronner-Fraser, 2007). Although the development of this tissue is poorly described, the first evidence of its formation is likely to be the expression of fibrillar collagen in the pharyngeal mesoderm of early larvae.…”

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

“…2, more detailed expression patterns are shown in Figs. S3-S7) (8,9). Interestingly, only FGF8/17/18, FGFA, and FGFE show transient expression in the presumptive mesoderm.…”

A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs

“…For instance, in the most basal chordate, the cephalochordate amphioxus, most neural plate border specifiers are found in the neural plate border whereas most neural crest specifiers, with the exception of Snail that is found in the neural tube, are expressed in the underlying mesoderm (Meulemans and Bronner-Fraser, 2005;Meulemans and Bronner-Fraser, 2007;Baker, 2008). It is possible that a group of genes forming the 'neural crest specifier module' was recruited by some cells in the neuroepithelial domain (future neural crest), whereas SoxE genes were co-opted simultaneously by presumptive neural crest and otic placode cells found in the same domain.…”