The Archipterygium hypothesis
In the middle of 19th century, Carl Gegenbaur (1876, 1878) proposed that the limbs might be derived from the gill arches based on observations in Chondrichthyes’ fins and in the archipterygial fins found in the Australian lungfish Neoceratodus forsteri (Krefft, 1870) (Kardong, 2012). He proposed that the archipterygial axis present in the fins corresponds to the extended gill radial and its gill arch would give rise to the pectoral girdle. It has also been reported that during the breeding season the male pelvic fin of Lepidosiren paradoxa (Fitzinger, 1837), also a lungfish, becomes a gill-like organ (reviewed by Foxon, 1933). Despite this being a seasonal change, it may reveal a developmental relationship between those structures.
Many genes are expressed in both gill arches and limbs in tetrapods. O’Rourke and Tam (2002) published an extensive review of the genes expressed in limb and branchial arch in the mouse. There are a numerous genes expressed in both organs belonging to different signaling pathways such as Fgf (fgf4, fgf8, fgf9, fgf10 and fgfr2), Shh (shh, gli1, gli2, gli3 and patch), Wnt (wnt5a and wnt11) and Bmp (bmp2, bmp4 and bmp7). In addition, there is a long list of shared transcription factors, which include: twist, dlx1, dlx2, dlx3, dlx5, dlx6, msx1, msx2, alk3, alk4, cart1, pitx1, gsc and mtsh.
Other examples are R-fng, bmp2 and fgf4, which are expressed in the ectoderm of the gill arch and in the apical ectodermal ridge (AER) of the limb (Tabin et al., 1999). The gene goosecoid (gsc) is expressed in the mesenchyme of both structures. Sonic hedgehog (shh), on the other hand, is expressed in the ectoderm of the branchial arch and in both the mesenchyme and ectoderm of the limb (Bouldin et al., 2010). Additional interesting cases are dlx1 and dlx2, these genes are expressed in the mesenchyme of the branchial arch and in the AER of the limb (Tabin et al., 1999).
Studies in the little skate Leucoraja erinacea (Mitchill, 1825) (Gillis et al., 2009), verified that gene expression patterns typical of the limb are found in the gill arches. shh is expressed in the epithelium covering the gill arch and its receptor ptc2 is expressed in the underlying mesenchyme. Meanwhile, fgf8 is expressed in the posterior region of the epithelium and has a regulatory feedback with shh. These patterns bear similarity with the expression of these genes during limb development. Furthermore, the exogenous application of retinoic acid (RA) or shh generates mirror duplication on the gill arch skeleton as it happens in the extremities. On the other hand, the gill arch of the ray has a ridge of pseudostratified epithelium, which closely resembles the AER of limb buds.
Shared gene expression between gill arches and developing extremities in different vertebrates supports the anatomical based hypothesis of Gegenbaur. However, a more systematic survey across different developmental pathways and vertebrate species is required.