Evolution of repeated structures along the body axis of jawed vertebrates, insights from the Scyliorhinus canicula Hox code

Abstract

The Hox gene family encodes homeodomain-containing transcription factors involved in the patterning of structures composed of repeated elements along the antero-posterior axis of Bilateralia embryos. In vertebrate, Hox genes are thought to control the segmental identity of the rhombomeres, the branchial arches, and the somites. They are therefore thought to have played a key role in the morphological evolution of structures like the jaw, girdles, and vertebrae in gnathostomes. Thus far, our knowledge about the expression patterns of the Hox genes, the Hox code, has been mainly restricted to osteichthyans species and little is known about chondrichthyans. Recently, we identified 34 Hox genes clustered in three complexes (HoxA, HoxB, and HoxD) in the dogfish (Scyliorhinus canicula) genome suggesting that in sharks most, if not all, genes belonging to the HoxC complex are lost. To gain insights into the evolution of gnathostome Hox transcription, we present here expression patterns along the anteroposterior axis for all Hox genes known in the dogfish. A comparison of these patterns with those of osteichthyans shows that the expression patterns of the Hox genes in serially homologous compartments such as the branchial arches, the hindbrain, and the somites underwent only subtle changes during the evolution of gnathostomes. Therefore, the nested expression of Hox genes in these structures, the Hox code, is a ground plan, which predates the morphological diversification of serially homologous structures along the body axis.

Tetrapod-like axial regionalization in an early ray-finned fish

“…A generally strong relationship between the regional identity and specific Hox expression domains in vertebrates would mean that the axial Hox domain pattern for Tarrasius matched that shared by tetrapods and sharks [2][3][4][5][6][7][8]22] (figure 2c), but not the anteriorized 'primitive' state of model actinopterygians (e.g. zebrafish) [18][19][20][21] (figure 2e).…”

“…In contrast, haemal arch placement, normally linked to the tail, appears fixed. They begin near the end of the body cavity and within the homologous sacral series in the digited tetrapod Acanthostega and the tetrapodomorph fish Eusthenopteron [13,17] ( figure 2a -c) and between the anterior expression limits of Hox11 (tetrapod sacral marker) and Hox12 (tetrapod caudal marker) paralogues in both the shark Scyliorhinus and the zebrafish Danio [18,22] (figure 2f ). In zebrafish, haemals can even be rib-bearing, a conjunction of elements also observed in the sacral and adjacent 'caudal' vertebra of Acanthostega [17,18] (figure 2f ).…”

“…This pattern is hypothesized by many researchers to be primitive for vertebrates and preclusive of tetrapod-like regionalization, particularly when combined with the lack of terrestrial selective regime [2,9,16,19 -22]. However, recent examination of Hox patterning in the shark Scyliorhinus has revealed a more tetrapod-than teleost-like distribution of domains, opening new possibilities for the jawed vertebrate ancestral state [22].…”

Why coelacanths are not ‘living fossils’

“…For example, we and other colleagues have recently found that serially homologous structures, that is, branchial arches, somites and rhombomeres, have undergone a high rate of morphological differentiation during gnathostome evolution, but show very few differences in Hox gene expression [38]. A key factor controlling the mutation rate is the effective genome size, i.e.…”

Penser la biologie dans un cadre phylogénétique

“…Cependant, il apparut bientôt que les poissons téléostéens, qui ont connu au moins une duplication supplémentaire de leur génome présentent (aux pertes secondaires près) au moins deux fois plus de complexes Hox que les tétrapodes [24]. Plus récemment, quatre complexes furent identifiés chez les chimères [25], mais trois seulement chez les requins et les raies [26,27]. L'analyse phylogénétique de ces résultats montre que l'ancêtre de tous les gnathostomes (y sur la Figure 4) possédait quatre complexes Hox.…”