Evidence that mechanisms of fin development evolved in the midline of early vertebrates

Abstract

The origin of paired appendages was a major evolutionary innovation for vertebrates, marking the first step towards fin- (and later limb-) driven locomotion. The earliest vertebrate fossils lack paired fins but have well-developed median fins, suggesting that the mechanisms of fin development were assembled first in the midline. Here we show that shark median fin development involves the same genetic programs that operate in paired appendages. Using molecular markers for different cell types, we show that median fins arise predominantly from somitic (paraxial) mesoderm, whereas paired appendages develop from lateral plate mesoderm. Expression of Hoxd and Tbx18 genes, which specify paired limb positions, also delineates the positions of median fins. Proximodistal development of median fins occurs beneath an apical ectodermal ridge, the structure that controls outgrowth of paired appendages. Each median fin bud then acquires an anteroposteriorly-nested pattern of Hoxd expression similar to that which establishes skeletal polarity in limbs. Thus, despite their different embryonic origins, paired and median fins utilize a common suite of developmental mechanisms. We extended our analysis to lampreys, which diverged from the lineage leading to gnathostomes before the origin of paired appendages, and show that their median fins also develop from somites and express orthologous Hox and Tbx genes. Together these results suggest that the molecular mechanisms for fin development originated in somitic mesoderm of early vertebrates, and that the origin of paired appendages was associated with re-deployment of these mechanisms to lateral plate mesoderm.

Noncanonical role of Hox14 revealed by its expression patterns in lamprey and shark

“…It is already known that posterior Hox genes (Abdominal-B group; Hox9-13) are coordinately expressed in the limb buds to establish the anteroposterior regional identities (5). This is also observed in the fin buds of chondrichthyans (17), suggesting that the Hox-code in the paired appendages, and that in the CNS and somites, was established before the divergence between chondrichthyans and osteichthyans (the rest of gnathostomes). In the lamprey, which lacks paired fins, Hox9 and Hox10 genes were shown to be expressed in the mesenchyme of dorsal fin fold (18).…”

“…The JTTϩIϩG 4 model was assumed (␣ ϭ 0.37). Support for critical nodes are shown in the order, posterior probabilities of the Bayesian analysis, support values of ML analysis using quartet-puzzling, and bootstrap probabilities of the neighbor-joining tree inference with 1,000 iterations (17). Note that the clustering of vertebrate Hox13 genes and tunicate Hox13 genes is not strongly supported.…”

Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons

“…Although the fossil record cannot unequivocally resolve the order of appearance of branchial rays and median fins, both appear before the origin of gnathostomes and paired appendages. Shared developmental gene expression patterns have previously been noted between gnathostome paired appendages and the unpaired median fins of chondrichthyans and lampreys, fueling the hypothesis that the paired fin patterning module was first assembled along the dorsal midline (41). However, the deep structural, functional, and regulatory similarities between paired appendages and the developing gill rays, and the antiquity of gills relative to appendages, allow us to suggest that the RA/Shh/Fgf8 signaling network had a plesiomorphic patterning function in gills before the origin of vertebrate appendages-a function that has been retained in the gill rays of extant chondrichthyans.…”

Development of the viscerocranial skeleton during embryogenesis of the sea lamprey,Petromyzon Marinus

“…A recent study suggests that developmental mechanisms patterning the branchial arches and paired fin skeletons are shared in vertebrates (Gillis et al, 2009). Considering the observation that the lamprey median fin may be patterned by similar mechanisms that regulate development of paired appendages (Freitas et al, 2006), it will be informative to determine the degree to which developmental mechanisms patterning the gnathostome branchial arches are conserved in lampreys (McCauley and Bronner-Fraser, 2004).…”