Development of oral and branchial muscles in lancelet larvae ofBranchiostoma japonicum

Abstract

The perforated pharynx has generally been regarded as a shared characteristic of chordates. However, there still remains phylogenetic ambiguity between the cilia-driven system in invertebrate chordates and the muscle-driven system in vertebrates. Giant larvae of the genus Asymmetron were reported to develop an orobranchial musculature similar to that of vertebrates more than 100 years ago. This discovery might represent an evolutionary link for the chordate branchial system, but few investigations of the lancelet orobranchial musculature have been completed since. We studied staged larvae of a Japanese population of Branchiostoma japonicum to characterize the developmental property of the orobranchial musculature. The larval mouth and the unpaired primary gills develop well-organized muscles. These muscles function only as obturators of the openings without antagonistic system. As the larval mouth enlarged posteriorly to the level of the ninth myomere, the oral musculature was fortified accordingly without segmental patterning. In contrast, the iterated branchial muscles coincided with the dorsal myomeric pattern before metamorphosis, but the pharynx was remodeled dynamically irrespective of the myomeric pattern during metamorphosis. The orobranchial musculature disappeared completely during metamorphosis, and adult muscles in the oral hood and velum, as well as on the pterygial coeloms developed independently. The lancelet orobranchial musculature is apparently a larval adaptation to prevent harmful intake. However, vestigial muscles appeared transiently with the secondary gill formation suggest a bilateral ancestral state of muscular gills, and a segmental pattern of developing branchial muscles without neural crest and placodal contributions is suggestive of a precursor of vertebrate branchiomeric pattern.

A new heart for a new head in vertebrate cardiopharyngeal evolution

“…The oral and velar muscles, in particular, share anatomical similarities with the oral and velar muscles of lampreys and hagfish (Fig. 4), although the pterygial muscles have a branchiomeric-like innervation pattern 99 . Gans 79 recognized this latter point and noted that this could mean that the branchiomeric muscles evolved before the last common ancestor (LCA) of vertebrates, as suggested by earlier authors 22 , but contrary to the original new head hypothesis 1 .…”

“…In the cephalochor-date amphioxus, the larval mouth and unpaired primary gills develop five groups of orobranchial muscles 99,100 . This musculature is anatomically reminiscent of the vertebrate branchiomeric muscles, and disappears through apoptosis during metamorphosis to give way to adult oral, velar and pterygial muscles 99 (Fig. 4), which are even more similar to vertebrate adult branchiomeric muscles.…”

Evolution of vertebrates as viewed from the crest

“…Pharyngeal segmentation is a trait of ancestral deuterostomes 102 , and unambiguous pharyngeal arch homologues with similar genetic controls are present in hemichordates, cephalochordates, and adult urochordates 100,102 , despite being secondarily lost in echinoderms 100,103 . Pharyngeal mesoderm also has a broad phylogenetic distribution, being present throughout chordates 104,105 . Neural crest derived cellular cartilage of vertebrates, rather than being a novelty of vertebrates 21 , instead appears have been coopted from cellular cartilage homologous to that present within the oral cirri of Cephalochordates 26 .…”

“…Neural crest cells secrete signals that derepress myogenesis, allowing formation of cranial myofibers 120 . These distinct myogenic regulatory subnetworks are thought to have arisen in early vertebrates concurrent with other cephalic modifications 118,120 , but have also been compared to muscle precursors in the amphioxus atrium 105 and potentially with visceral musculature of protostomes 121 . Vertebrate cranial muscle patterning, differentiation, and organization might require regulatory control that arose from novel interactions with neural crest (See Fig.…”

Gene regulatory networks and cell lineages that underlie the formation of skeletal muscle

“…The cephalochordate Amphioxus has somites, where a Pax3/7 gene homolog (42) is expressed, and forms myotomal muscles with expression of two MyoD family genes (43). It has branchiomeric head muscles analogous to those of jawless fish (44), which are lost at metamorphosis and then reformed in the adult. However, their formation appears to be independent of myogenic regulatory genes, expressed exclusively in somites (43).…”