Development of hypobranchial muscles with special reference to the evolution of the vertebrate neck
© The Author(s). 2018
Received: 28 October 2017
Accepted: 6 February 2018
Published: 18 February 2018
The extant vertebrates include cyclostomes (lamprey and hagfish) and crown gnathostomes (jawed vertebrates), but there are various anatomical disparities between these two groups. Conspicuous in the gnathostomes is the neck, which occupies the interfacial domain between the head and trunk, including the occipital part of the cranium, the shoulder girdle, and the cucullaris and hypobranchial muscles (HBMs). Of these, HBMs originate from occipital somites to form the ventral pharyngeal and neck musculature in gnathostomes. Cyclostomes also have HBMs on the ventral pharynx, but lack the other neck elements, including the occipital region, the pectoral girdle, and cucullaris muscles. These anatomical differences raise questions about the evolution of the neck in vertebrates.
In this study, we observed developing HBMs as a basis for comparison between the two groups and show that the arrangement of the head–trunk interface in gnathostomes is distinct from that of lampreys. Our comparative analyses reveal that, although HBM precursors initially pass through the lateral side of the pericardium in both groups, the relative positions of the pericardium withrespect to the pharyngeal arches differ between the two, resulting in diverse trajectories of HBMs in gnathostomes and lampreys.
We suggest that a heterotopic rearrangement of early embryonic components, including the pericardium and pharyngeal arches, may have played a fundamental role in establishing the gnathostome HBMs, which would also have served as the basis for neck formation in the jawed vertebrate lineage.
Morphologically, cyclostomes do not have an evident neck domain, as the occipital region, shoulder girdle, and cucullaris muscles are not present in these animals [3, 16]. In contrast, both lampreys and hagfishes have HBMs on the ventral part of the pharynx; these are innervated by the homologue of the hypoglossal nerve (Fig. 1a) [3, 17]. However, these muscles lie superficial to the pharynx, not inside the mouth and pharynx as they do in the gnathostomes [18, 19]. These anatomical disparities raise questions about the evolutionary origins of the neck in gnathostomes; however, the mechanisms leading to these disparities remain largely unknown.
The anatomical elements constituting the neck originate in the vicinity of the head–trunk interface of gnathostome embryos. The interface consists of the anterior extremity of somites and the posterior extremity of pharyngeal arches, and the circumpharyngeal crest cells pass through this interfacial domain (Fig. 1b) [1, 20]. Notably, the anterior occipital somites and circumpharyngeal crest cells give rise to HBMs and their connective tissues, respectively [4, 21, 22] also see below); thus, the interfacial domain is a key embryonic region for understanding neck morphogenesis .
As noted, although anatomical disparities exist between cyclostomes and gnathostomes, a number of embryological studies have observed resemblances in the head–trunk interface and HBMs. For example, it has been shown that the lamprey embryo also possesses the interfacial domain [16, 23]. Studies have revealed that the occipital somites give rise to HBM precursors, which migrate once posterior to the pharyngeal arches and then turn rostrally to reach the ventral pharynx in vertebrates, including the lamprey [4, 9, 22, 24–33]. Molecular analyses have revealed the involvement of Pax3, a paired box transcription factor-encoding gene, in the development of HBMs [26, 28, 29, 34]. Similarly, lamprey HBMs are marked by Pax3/7, a homolog of Pax3 . Thus, cyclostomes and gnathostomes have similar embryonic components and diverse anatomical outcomes in the head–trunk interface. This suggests that developmental differences of components in the interfacial domain account for the anatomical disparities between the two groups, and comparative embryological analysis of this domain is crucial to understanding vertebrate neck evolution . The analysis of HBMs is especially crucial, as muscles found in both groups would be a useful developmental landmark for comparing the interfacial domains in these animals. However, no detailed comparison of the HBM pathway between lamprey and gnathostome embryos has been reported to date. Furthermore, the migration trajectory of HBMs relative to the pharynx remains obscure, even in embryos of gnathostomes. In the present study, we investigated the development of HBMs and the embryonic morphology of the head–trunk interface in chicken, mouse, shark, and lamprey embryos to gain insight into the evolution of the vertebrate neck.
Mature adult lampreys (Lethenteron camtschaticum, synonym for Lethenteron japonicum) were collected in Hokkaido, Japan, and the fertilized eggs were obtained as described previously . Adult cloudy catsharks (Scyliorhinus torazame) were captured in Ibaraki, Japan. They laid fertilized eggs in saltwater tanks and the eggs were incubated at 16 °C. Fertilized chicken eggs (Gallus gallus) were purchased from local suppliers and incubated at 38 °C. C57BL/6 mouse embryos (Mus musculus) were obtained from CDB animal facilities. Wnt1-Cre heterozygous mice  and R26R-H2B-EGFP homozygous mice (Acc No. CDB0203K: http://www2.clst.riken.jp/arg/reporter_mice.html)  were crossed and the offspring were genotyped by PCR to obtain Wnt1-Cre/R26R-H2B-EGFP embryos. Noon on the day that the vaginal plug was observed was defined as E0.5. Embryos of lamprey, shark, chicken, and mouse were staged, following the systems described in [39–42], respectively.
Histological analysis and 3D reconstruction
Lamprey and shark embryos were fixed in Bouin’s fixative, sectioned, and stained as described previously . At least three embryos were observed for each developmental stage. Carazzi’s hematoxylin was used for lamprey sections, Mayer’s hematoxylin for shark sections, and Alcian blue for cartilaginous staining. 3D reconstruction of embryos was performed by the method described previously .
Molecular cloning and phylogenetic analysis
Embryonic total RNA was extracted by TRIzol Reagent (Life Technologies), and cDNA was synthesized by SuperScript IV Reverse Transcriptase (Thermo Fisher Scientific). RNA-sequence analysis of embryonic lamprey and shark was performed and the sequences of lamprey Nkx2–3/2–5/2–6, Tbx1/10A, and Tbx4/5, and shark Nkx2–5 and Tbx5 were found in the assembled data set (to be published elsewhere). DNA fragments were amplified, cloned, and sequenced as described previously . The accession numbers and primers used in this study are listed in the Additional file 1. The sequences of lamprey DlxB, Hox2α, Hox3α, and Pax3/7, and shark Dlx5, Pax3, and Tbx1 have been described previously [35, 44–48]. Shark Hoxa2 sequence has been described recently in a separate study (Pascual-Anaya et al., under preparation) and is publicly available in GenBank under the accession number MF398238. For phylogenetic analyses, amino acid sequences of orthologous genes’ from different vertebrate species were compiled from GenBank (http://www.ncbi.nlm.nih.gov/) and Ensembl (http://www.ensembl.org/index.html). Multiple alignment of protein sequences were performed with MAFFT  as implemented at the European Bioinformatics Institute’s web server (http://www.ebi.ac.uk/Tools/msa/mafft/), or MUSCLE  as implemented in MEGA v7 , release 7,161,111-i38651, with default parameters, and saved in FASTA format. Resulting alignments were then trimmed by trimAl version 1.2rev59  using the ‘–automated1’ parameter and then formatted into NEXUS format by readAl v.1.2 (bundled with the trimAl package) (Suppl. Molecular phylogenetic trees of lamprey were inferred using Bayesian inference with MrBayes 3.2.6  under the assumption of an LG + I + G evolutionary model and were performed with two independent MrBayes runs, 4 chains each. Convergence was considered when the standard deviation < 0.01 for more than 1 million generations. To build the consensus tree, a burn-in of the 25% of the trees was performed (see Additional file 1: Figure S1 for the number of generations of each gene’s phylogenetic analysis).
In situ hybridization
Lamprey and shark embryos were fixed in MEMFA fixative. Chicken and mouse embryos were fixed in 4% PFA/PBS. Whole-mount in situ hybridization was performed as described in . The method of two-color whole-mount in situ hybridization has been described by . Embryos were imaged using a Leica MZ16FA. After whole-mount in situ hybridization, lamprey embryos were immersed in MEMFA fixative with 2.5% glutaraldehyde solution, dehydrated, and embedded in paraffin. Sections were prepared at 6 μm, and counterstained in eosin solution. The protocol of in situ hybridization on shark sections was described in . Adjacent paraffin sections were used to compare gene expression patterns. Sections were imaged with an Olympus BX53. The expression pattern of each gene was investigated in > 3 embryos.
Three Wnt1-Cre/R26R-H2B-EGFP embryos were obtained and utilized in the analysis. The embryos were fixed in 4%PFA/PBS, dehydrated, and embedded in paraffin. Sections were prepared at 6 μm. Deparaffinized sections were autoclaved in 1 mM citrate buffer (pH 6.0) to unmask epitopes . Anti-PAX3 mouse monoclonal antibody (1/100 dilution, ab69856, Abcam) and anti-GFP rabbit polyclonal antibody (1/500 dilution, ab290, Abcam) were used for the primary antibody. Goat anti-mouse IgG Alexa Fluor 647 (1/200 dilution, A21237, Thermo Fisher Scientific) and goat anti-rabbit IgG Alexa Fluor 488 (1/500 dilution, A11034, Thermo Fisher Scientific) were used for the secondary antibody. The signal detection was performed with a confocal laser microscope Leica TCS SP8X and Spectral Dye Separation in LAS AF software.
Development of HBMs in jawed vertebrate embryos
Subsequently, these precursors reached to the lateral side of the anterior pericardium at HH23 and E10.5 (Fig. 2b, d–f). In these embryos, the pericardium was commonly located ventral to the pharynx, and the rostral tip of HBMs appeared to have penetrated the medial side of the hyoid arch (Fig. 2e, f). This medial extension of HBM precursors was also suggested by the expression pattern of Myf5, which marks both cranial and trunk myoblasts (Fig. 2a–d).
We next explored the developmental pathway of HBMs in the cloudy catshark, S. torazame, to test whether the trajectory of HBM precursors is shared in crown gnathostomes. We performed 3D reconstruction of shark embryos from the otic vesicle to heart levels (Additional file 1: Figures S3a and S4). Shark mesoderm, which exhibits an epithelialized, not mesenchymal, state at early stages [43, 58], is a useful model for observing HBMs in gnathostomes.
By stage 27, HBM precursors had descended around the posterior edge of the branchial arches to form the hypoglossal cord  on each side of the pericardium. The rostral tip of the cord had reached to the level of the fourth branchial arch (Fig. 4b).
At stage 29, the HBM precursors extended medially at the level of the hyoid arch. Notably, its anterior part was embraced laterally and ventrally by the intermandibularis and interhyoideus muscles, while the posterior remained ventral to the branchial arches (Fig. 4c, d). Crucially, this topographical relationship of HBMs and pharyngeal arches in this species perfectly coincided with that of chicken and mouse (Figs. 2, 3 and 4). The HBM precursors branched out to form the coracohyoideus and coracobranchialis muscles on both sides of the ventral aorta and pericardium, and subsequently, the majority of the HBMs were found inside gill muscles and cartilages (interhyoideus and constrictor superficialis muscles, ceratohyal, epibranchial, and ceratobranchial cartilages), as seen in the adult shark (Fig. 4c, d, and Additional file 1: Figure S4).
Development of HBMs in the lamprey
To compare the developmental trajectory of HBMs between cyclostomes and gnathostomes, we observed the development of the Arctic lamprey, L. camstchaticum (Additional file 1: Figures S3b and S6). The youngest lamprey embryos examined in histological analysis were at Tahara’s stage 26 , when yolk granules were substantially reduced. Each of the pharyngeal arches possessed branchial mesoderm, which was located anterior to the pericardial mesoderm, immediately below the axial mesoderm (Figs. 4e, 5d–f, and Additional file 1: Figure S6a, e). This topology of the pharyngeal mesoderm and pericardium was also observed in earlier stages of lamprey embryos (Additional file 1: Figure S7). Thus, the relative position of the pericardium posterior to the pharynx contrasts with that in gnathostomes (Additional file 1: Figures S5 and S7). Signs of HBM development in the lamprey were first observed on the ventrolateral edge of somites, above the pericardial mesoderm (Fig. 4e and Additional file 1: Figure S6a, e, j-k').
During stages 27 and 28, the HBM precursors on both sides extended ventrally between the ectoderm and the pericardial mesoderm as several streams of cell populations (Fig. 4f and Additional file 1: Figure S6). These streams later converged ventroanteriorly to form the hypoglossal cord , which expands from the lateral side of the pericardium to the posterior branchial arches (Fig. 4f, g). Although the trajectory of these HBMs spreading on the lateral side of the pericardium is similar to that in gnathostomes, the lamprey HBMs uniquely developed along the ventrolateral aspect of the branchial arches (no longer in the pericardial mesoderm as in gnathostomes), differing clearly from those in gnathostomes (Figs. 2, 3 and 4).
By stage 30, HBM precursors developed further anteriorly up to the otic level and resided ventrolaterally to the pharyngeal muscles and skeletons, including mandibular and hyoid arches (Fig. 4g and Additional file 1: Figure S6). This relative position of HBMs and the pharynx is comparable with that in the adult lamprey.
Trajectory of the HBMs relative to pharyngeal arches
To show the distribution of HBMs and pharyngeal arches in shark and lamprey embryos more clearly, we performed in situ hybridization using orthologous genes of Pax3 and Dlx5, as well as Tbx1, which is expressed in the head mesoderm of pharyngeal arches, and Hox genes, which mark ectomesenchymal cells in the pharyngeal arches (Additional file 1: Figure S1) [35, 44, 45, 47, 59].
Taken together, these results are consistent with our histological observations, indicating that shark HBM precursors pass outside of the pericardium and expand inside the pharynx at the level between the hyoid and first branchial arches, whereas in lamprey HBM precursors remain outside the pericardium and pharyngeal arches. Thus, although the initial avoidance of the branchial region and the lateral migration to the pericardium are likely to be steps in a conserved developmental program in the entire vertebrate HBMs [9, 24, 27, 30, 31], the trajectory of HBMs internalized at the hyoid level is a shared trait only for crown gnathostomes (Figs. 2, 3, 4, 6 and 7).
In this study, we show that HBM precursors travel along the head trunk interface, namely, along the posterior edge of the postotic pharyngeal arches and lateral to the pericardium in both crown gnathostomes and lampreys, while the topographical relationship of the pericardium to the pharynx and the trajectory of HBMs in the ventral pharynx differ substantially between the two groups. In the gnathostomes, the pericardium lies ventral to the pharyngeal arches, and the HBM precursors intrude inside the hyoid and mandibular arches (Figs. 2, 3, 4, 6). In contrast, in the lamprey, the pericardium is located caudal to the pharynx, and the HBM precursors extend outside of the pharyngeal muscles and skeletons (Figs. 2, 7). These observations provide unique insights into the evolution of the head–trunk interface as discussed below.
These findings indicate that the pericardium is tightly coupled with the development of HBMs in vertebrates. This linkage suggests that the position of the gnathostome pericardium may permit the HBM precursors to circumvent branchial arches ventrally and project medially into the hyoid arch to reach the inside of the mouth (Fig. 8). This trajectory is absent in the lamprey and inconceivable in the embryos given the position of the lamprey pericardium, which does not attach to the mandibular and hyoid arches (Figs. 4, 5, 7 and 8). Therefore, a heterotopic shift of pericardium relative to the pharynx may underlie a trajectory change of the HBMs.
The above discussion implies a morphological transition of the head–trunk interfacial domain from one state to another in vertebrate phylogeny. The prevalence of the pericardium, pharynx, and HBMs in extant vertebrates suggests the presence of those embryonic elements in a common ancestor of cyclostomes and gnathostomes, although the arrangement of ancestral elements remains unknown. In this regard, information from paleontology is important to speculate about the ancestral condition.
Some fossil jawless vertebrates, such as Achanarella, Anaspida, and Jamoytius, possess the posteriorly elongated branchial apparatus with a number of gill openings [60, 61], and trunk scales or myomeres dorsal to the branchial region [61–63], but lack apparent occipital and shoulder elements. These morphological features are shared by the interfacial domain of modern cyclostomes, although the hagfish likely represents a derived condition in the hypoglossal nerve and HBMs as well [1, 17].
It is difficult to speculate with confidence on the anatomy of the head–trunk interface and HBMs in other fossil jawless vertebrates, such as Heterostracans, Galeaspids and Osteostracans, because data on their soft tissue morphology are very rare, insights into their internatl anatomy must be gleaned mainly from endo- and exoskeletons . Of these fossil species, Osteostracans have an ossified pericardium attached to the postbranchial wall, and the pericardium and posterior gills are positioned in the same longitudinal axis [60, 64]. They also possess the pectoral girdle, and possibly paired common cardinal veins (the ducts of Cuvier) just behind the postbranchial wall, suggesting a gnathostome-like condition of the head–trunk interface in this animal [54, 65, 66]. Thus, it may be conceivable that HBMs of Osteostracans are positioned on the ventral aspect of the pharynx, separated from the dorsal muscle mass, and caudally attached to the pectoral girdle, or possibly to the ventral bridge of dermal bone located ventral to the pericardium . The morphology of anterior HBMs and their position relative to the gill elements are difficult to assume, and further analyses of this fossil will be required. In contrast, placoderms display muscle attachment sites for HBMs on the lower jaw and shoulder skeletons, which are comparable with those of extant gnathostomes .
Given the current phylogenetic positions of the abovementioned fossil vertebrates [63, 68], these observations suggest that the head–trunk interface found in the lamprey embryo may represent the ancestral condition, and a rearrangement of preexisting embryonic components in the ancestral vertebrate may have occurred during the transition from jawless to jawed vertebrates (Fig. 8c). Thus, we hypothesize that a heterotopic shift of the pericardium together with a gain of an internal trajectory of HBM precursors, was a key embryonic change for the evolution of the gnathostome HBMs, which function as jaw opening and tongue muscles (Fig. 8c) [7, 11, 13, 14]. Furthermore, this rearrangement may have contributed to the establishment of the gnathostome head–trunk interface, which provides the basis for the development of the jawed vertebrate neck.
In our comparative embryological analyses, we found that the pericardium was posterior to the pharynx and HBM precursors extended outside of those elements in the lamprey, whereas the pericardium was ventral to the pharynx and HBM precursors traveled outside of the pericardium and inside the hyoid and mandibular arches in crown gnathostomes. Based on current paleontological data on stem gnathostomes, we hypothesize that the embryonic arrangement of the pericardium, pharynx, and HBM precursors likely underwent a transition from the lamprey condition to the crown gnathostome condition, which was a key embryonic change not only for the establishment of the head–trunk interface, but also for the evolution of the neck in jawed vertebrates.
We thank K. Shirato for shark fishing, S. Shibuya, K. Yamamoto, and E. Momota for the maintenance of lampreys and shark. Drs. F. Sugahara, R. Kusakabe, S. Kuroda, W. Takagi, Y. Kageyama, and Y Nakai were engaged in sampling of lamprey and shark embryos. Drs. H. Nagashima and M. Takechi helped mouse and chicken sampling. Drs. H. Kiyonari, K. Inoue, S Nishikawa and W. Hsu helped transgenic mouse preparation. RIKEN Kobe Light Microscopy Facility supported the imaging experiments. Dr. Sansom kindly gave advice on fossils. We thank Drs. F. Sugahara, J. Pieretti and T. Onai for discussions and critical reading of the manuscript.
This work was supported in part by a Grant-in-Aid for Scientific Research (A) 15H02416, Grant-in-Aid for Scientific Research on Innovative Areas 17H06385, and a Naito Grant for the Promotion of Focused Research (The Naito Foundation) to S.K.
Availability of data and materials
All sequences generated in this study are publicly available in NCBI GenBank under the accession numbers LC331563-LC331566 and LC333760.
NA and SK designed the research. NA, JP-A, SH, and TH performed molecular experiments. NA, JP-A, and SK wrote the paper. All authors read and approved the manuscript.
All animal experiments were carried out with the approval of the Institutional Animal Care and Use Committee of RIKEN, Kobe Branch.
Consent for publication
The authors declare that they have no competing interests.
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