Evolutionarily conserved morphogenetic movements at the vertebrate head–trunk interface coordinate the transport and assembly of hypopharyngeal structures

Abstract

The vertebrate head–trunk interface (occipital region) has been heavily remodelled during evolution, and its development is still poorly understood. In extant jawed vertebrates, this region provides muscle precursors for the throat and tongue (hypopharyngeal/hypobranchial/hypoglossal muscle precursors, HMP) that take a stereotype path rostrally along the pharynx and are thought to reach their target sites via active migration. Yet, this projection pattern emerged in jawless vertebrates before the evolution of migratory muscle precursors. This suggests that a so far elusive, more basic transport mechanism must have existed and may still be traceable today.Here we show for the first time that all occipital tissues participate in well-conserved cell movements. These cell movements are spearheaded by the occipital lateral mesoderm and ectoderm that split into two streams. The rostrally directed stream projects along the floor of the pharynx and reaches as far rostrally as the floor of the mandibular arch and outflow tract of the heart. Notably, this stream leads and engulfs the later emerging HMP, neural crest cells and hypoglossal nerve. When we (i) attempted to redirect hypobranchial/hypoglossal muscle precursors towards various attractants, (ii) placed non-migratory muscle precursors into the occipital environment or (iii) molecularly or (iv) genetically rendered muscle precursors non-migratory, they still followed the trajectory set by the occipital lateral mesoderm and ectoderm. Thus, we have discovered evolutionarily conserved morphogenetic movements, driven by the occipital lateral mesoderm and ectoderm, that ensure cell transport and organ assembly at the head–trunk interface.

Expansion of the neck reconstituted the shoulder–diaphragm in amniote evolution

“…This passive positional shift of the muscle precursors of the diaphragm is another example of the musculoskeletal development being affected by morphogenetic movements of embryonic bodies (Lours‐Calet et al . ).…”

“…The muscle precursor cells have already migrated into the pleuroperitoneal fold before the caudal transposition of the heart (E10.5; Dietrich et al 1999), thus allowing them to later differentiate within the pleuroperitoneal fold at the proper position. This passive positional shift of the muscle precursors of the diaphragm is another example of the musculoskeletal development being affected by morphogenetic movements of embryonic bodies (Lours-Calet et al 2014).…”

Neural crest and the patterning of vertebrate craniofacial muscles

“…It is well known from comparative studies that the head:trunk interface has undergone profound evolutionary changes during vertebrate evolution (reviewed by: Sefton, Bhullar, Mohaddes, & Hanken, ). Among these is the location of pectoral girdle elements, many of which initially were close to and stabilized upon an expanded dermal roof of the skull and located at the same axial levels as caudal branchial muscles and NC‐derived gill elements (reviewed by: Ferguson & Graham, ; Lours‐Calet et al, ; Oisi et al, ; Sefton et al, ), but in amniotes arise from more caudally located somites and somatic mesoderm (reviewed by Nagashima et al, ).…”

“…found evolutionary changes during vertebrate evolution (reviewed by:Sefton, Bhullar, Mohaddes, & Hanken, 2016). Among these is the location of pectoral girdle elements, many of which initially were close to and stabilized upon an expanded dermal roof of the skull and located at the same axial levels as caudal branchial muscles and NC-derived gill elements (reviewed by:Ferguson & Graham, 2004;Lours-Calet et al, 2014;Oisi et al, 2015;Sefton et al, 2016), but in amniotes arise from more caudally located somites and somatic mesoderm (reviewed byNagashima et al, 2016).Using transgenic mice in which mesoderm or NCr cells carried lineage markers,Matsuoka et al (2005) identified clusters of branchial NCr-derived cells on both the supraoccipital bone and the scapular spine, at sites where the trapezius attaches. These results suggest that the tight, obligatory partnering that defines intra-branchial myogenesis holds true for those myoblasts that exit the arches.…”

Involvement of HGF/MET signaling in appendicular muscle development in cartilaginous fish

“…Splotch mutants, mice deficient in Pax3 , lack the expression of Lbx1 at the ventral edge of the dermomyotome and fail to form a pool of migratory muscle precursors. Thus, Splotch mice lack the muscles derived from migratory muscle precursors, including limb muscles and diaphragm (Lours‐Calet et al., ; Mennerich et al., ). Pax3 also regulates the expression of c‐Met , which encodes a tyrosine kinase receptor and is expressed in the ventral edge of the dermomyotome, as well as in the muscle precursors migrating toward the targets (Adachi et al., ; Bladt et al., ; Dietrich et al., ; Haines et al., ; Scaal et al., ).…”