Mode of reduction in the number of pharyngeal segments within the sarcopterygians

Abstract

BackgroundPharyngeal segmentation is a defining feature of vertebrate embryos and is apparent as a series of bulges found on the lateral surface of the embryonic head, the pharyngeal arches. The ancestral condition for gnathostomes is to have seven pharyngeal segments: jaw, hyoid, and five posterior branchial arches. However, within the sarcopterygians, the pharyngeal region has undergone extensive remodelling that resulted in a reduction in the number of pharyngeal segments, such that amniotes have only five pharyngeal arches. The aim of this study is to probe the developmental basis of this loss of pharyngeal segments.ResultsWe have therefore compared the development of the pharyngeal arches in an amniote, the chick, which has five segments, with those of a chondrichthyan, the catshark, which has seven segments. We have analysed the early phase of pharyngeal segmentation and we find that in both the most anterior segments form first with the posterior segments being added sequentially. We also documented the patterns of innervation of the pharynx in several vertebrates and note that the three most anterior segments receive distinct innervation: the first arch being innervated by the Vth nerve, the second by the VIIth and the third by the IXth. Finally, we have analysed Hox gene expression, and show that the anterior limit of Hoxa2 aligns with the second pouch and arch in both chick and catshark, while Hoxa3 is transiently associated with the third arch and pouch. Surprisingly, we have found that Hoxb1 expression is spatially and temporally dynamic and that it is always associated with the last most recently formed pouch and that this domains moves caudally as additional pouches are generated.ConclusionWe propose that the first three pharyngeal segments are homologous, as is the posterior limit of the pharynx, and that the loss of segments occurred between these two points. We suggest that this loss results from a curtailment of the posterior expansion of the pharyngeal endoderm in amniotes at relatively earlier time point, and thus the generation of fewer segments.

A reappraisal and revision of the numbering of the pharyngeal arches

“…Our recent studies have highlighted homologous features of the posterior limit of the pharyngeal arches across the vertebrates (Shone et al 2016). It has been shown that the most posterior pouch is marked by expression of HOX1.…”

“…It has been shown that the most posterior pouch is marked by expression of HOX1. Thus, in lampreys, it is the 8th pouch that expresses LjHox1w (Takio et al 2007), in the catshark the 6th pouch expresses HoxB1, and in amniotes, chick and mouse, it is the 4th pouch that expresses HoxB1 (Shone et al 2016). Additionally, in all vertebrates, the posterior margin of the pharynx is skirted by the hypoglossal (XIIth) nerve and the fourth pouch is the site of origin of the ultimobranchial body (Kardong, 2012;Shone et al 2016).…”

“…The other reason is that this numbering reflects evolutionary considerations. The ancestral state for tetrapods is to have six pharyngeal arches (Shone et al 2016), numbered 1, 2, 3, 4, 5 and 6, and this is the situation seen in anurans and urodeles. However, in amniotes the number of arches was reduced to five but the terminal arch is still labelled the '6th' to imply homology with the last most posterior 6th arch of amphibia.…”

Launch of Zoological Letters

“…Kishida et al (2015), for example, have demonstrated that baleen whales lost the dorsal domain of the olfactory bulb, known to induce innate avoidance behavior against odors of predators and spoiled foods, before the toothed and baleen whale split based on not only whole genome sequences but also fossil data, indicating that profound changes in the chemosensory capabilities had occurred in the cetacean lineage during the period when ancestral whales migrated from land to water. Shone et al (2016) evaluated fossil agnathan morphological traits to speculate about an evolutionary sequence in vertebrate gill number. Suzuki et al (2016) referred to placoderm fossil data (Young, 2008) in suggesting that vertebrate extrinsic eye muscles adhere to ancestral anatomical patterns.…”

Hox-mediated endodermal identity patterns the pharyngeal muscle formation in the chordate pharynx

“…Hox genes are thought to play important roles in establishing the regional identity of the pharynx along the AP axis (Couly et al, 1998;Gendron-Maguire et al, 1993;Hunt et al, 1991;Rijli et al, 1993). In the pharyngeal endoderm, Hox genes also exhibit coordinated expression during vertebrate development (Shone et al, 2016). In mice, loss of Hoxa1 and Hoxb1 functions results in absence of the third pharyngeal pouch derivatives, such as the thymus and parathyroid (Rossel and Capecchi, 1999).…”