Morphogenetic mechanism of the acquisition of the dinosaur-type acetabulum

Abstract

Understanding morphological evolution in dinosaurs from a mechanistic viewpoint requires the elucidation of the morphogenesis that gave rise to derived dinosaurian traits, such as the perforated acetabulum. In the current study, we used embryos of extant animals with ancestral- and dinosaur-type acetabula, namely, geckos and turtles (with unperforated acetabulum), and birds (with perforated acetabulum). We performed comparative and experimental analyses, focusing on inter-tissue interaction during embryogenesis, and found that the avian perforated acetabulum develops via a secondary loss of cartilaginous tissue in the acetabular region. This cartilage loss might be mediated by inter-tissue interaction with the hip interzone, a mesenchymal tissue that exists in the embryonic joint structure. Furthermore, the data indicate that avian pelvic anlagen is more susceptible to paracrine molecules, e.g. Wnt ligand, secreted by the hip interzone than ‘reptilian’ anlagen. We hypothesize that during the emergence of dinosaurs, the pelvic anlagen became susceptible to the Wnt ligand, which led to the loss of the cartilaginous tissue and to the perforation in the acetabular region. Thus, the current evolutionary-developmental biology study deepens our understanding of morphological evolution in dinosaurs and provides it with a novel perspective.

The Avian Acetabulum: Small Structure, but Rich with Illumination and Questions

“….resembled early ancestral/developmental morphologies (that is, instances of localized paedomorphosis): the broad, flat avian ischium resembled the early embryonic state and that of ancestral archosaurian [my emphasis] condition more than it did the intermediate dinosaurian conditions." It should be noted in passing that although studies like those of Egawa et al [122], Griffin et al [20], and many others [127][128][129][130] exhibit a surprisingly Haeckelian recapitulationism, the data they provide are more reasonably interpreted in accordance with von Baer's principles of simple conservativism of early embryos, without the orthogenetic implications of Haeckel's recapitulation of past ancestors. In the words of Paul Ehrlich and colleagues: "The resemblance of early vertebrate embryos is readily explained without resort to mysterious forces compelling each individual to reclimb its phylogenetic tree."…”

“…In the case of quail, not only were the acetabula imperforate throughout embryogenesis, but even the adult acetabulum may be almost closed (Figure 5d). Egawa et al [122] further suggested that a dinosaur-type perforated acetabulum arises from acetabular cartilage loss in chicken embryos. They linked acetabular perforation in "non-avian" dinosaurs and birds (represented in their study by Struthio and Gallus) with high susceptibility to bone morphogenetic protein (BMP) antagonists and Wnt ligands [122].…”

“…Egawa et al [122] further suggested that a dinosaur-type perforated acetabulum arises from acetabular cartilage loss in chicken embryos. They linked acetabular perforation in "non-avian" dinosaurs and birds (represented in their study by Struthio and Gallus) with high susceptibility to bone morphogenetic protein (BMP) antagonists and Wnt ligands [122]. They point out that in non-archosauromorph sauropsids with unperforated adult acetabula, the pelvic anlagen are not susceptible to the joint-secreted molecules, whereas in the transition to non-dinosaurian archosauromorphs with unperforated acetabula in the adult, the pelvic anlagen became susceptible to BMP antagonists but less susceptible to Wnt ligands, leading to no cartilage loss.…”

“…Egawa et al [122] argue that many anatomical landmarks in birds show developmental timing that parallels their phylogenetic order of acquisition, a Haeckelian interpretation, implying that the process of terminal addition may play a major role in ontogeny. Yet, so-called "terminal addition" is nothing more than the end of the epigenetic landscape, whether in or out of the eggshell, and most vertebrates have considerable additions following hatching in birds or birth in mammals (note especially marsupials where the premature fetus will finish much of its ontogeny within the marsupium with a mouth attached to the nipples).…”

The dinosaurian femoral head experienced a morphogenetic shift from torsion to growth along the avian stem

“…Additionally, in adults of extinct dinosaurs the relative size of acetabular perforation gradually diminished in size towards ornithurans [ 11 ]. Embryonic joint spaces have special mesenchymal layers called the interzone (IZ), which spans the acetabulum in embryonic saurian hip joints, and IZ-expressed molecules (canonical Wnt ligands) cause the perforation of the avian acetabulum [ 84 ]. Therefore, that the evolutionary reduction of adults' acetabular size probably reflects a reduction of the IZ range and thus, that of the acetabulum of embryos.…”