Symposium on the evolution and development of the vertebrate head

Among the symposia held at the seminal meeting of the European Society for Evolutionary Developmental Biology was one centered on the development and evolution of the vertebrate head, an exquisitely complex anatomical system. The articles presented at this meeting have been gathered in a special issue of the Journal of Experimental Zoology, and are here reviewed by the organizers of the symposia. These articles cover a breadth of subjects, including interactions between cells derived from the different germ layers, such as those underlying neural crest cell migration and fate and cranial muscle specification, as well as placode development and the origin, development, and evolution of important evolutionary innovations such as jaws and the trabecula cranii. In this introduction, we provide a short historical overview of themes of research into the fundamental organization, structure, and development of the vertebrate head, including the search for head segmentation and the relevance of the New Head Hypothesis, and subsequently present the topics discussed in each of the articles. This overview of the past and the present of head evo-devo is then followed by a glimpse at its possible future and a brief examination of the utility of the notions of heterochrony, heterotopy, and heterofacience in describing evolutionarily important changes in developmental events.     

An evaluation of head position and craniofacial reference line variation

Natural head position (NHP) is the usual, balanced position of the head which is adopted for viewing the horizon or an object at eye level. Determination of NHP is useful when reconstructing facial form in art, forensics, orthodontic diagnosis and treatment planning for surgical management of craniofacial dysmorphic conditions. When NHP is uncertain, correction such as orientation to Frankfurt horizontal (FH) has been advocated. However, FH angulation varies between individuals and is subject to landmark identification error. Previous studies have measured FH and other craniofacial planes in relation to the true horizontal (HOR) with subjects in NHP and have found similar variation to that found with FH. This study measured craniofacial planes in 40 Aboriginal Australians (20 male, 20 female, aged 17 years or greater) from lateral cephalographs and compared its results with classical previous studies. Four planes, the neutral horizontal axis (NHA), FH, Krogman-Walker line (KW line), and palatal plane (P plane) demonstrated near parallelism and averaged between −1° and −2° from HOR. The combined use of NHA, FH, KW line, and P plane enables more effective corrected head position (CHP).     

Patterning of avian craniofacial muscles

Vertebrate voluntary muscles are composed of myotubes and connective tissue cells. These two cell types have different embryonic origins: myogenic cells arise from paraxial mesoderm, while in the head many of the connective tissues are formed by neural crest cells. The objective of this research was to study interactions between heterotopically transplanted trunk myotomal cells and presumptive connective tissue-forming cephalic neural crest mesenchyme. Presumptive or newly formed cervical somites from quail embryos were implanted lateral to the midbrain of chick hosts prior to the onset of neural crest emigration. Hosts were sacrificed between 7 and 12 days of incubation, and sections examined for the presence of quail cells. Some grafted tissues differentiated in situ, forming ectopic skeletal, connective, and muscle tissues. However, many myotomal cells broke away from the implant, became integrated into adjacent neural crest mesenchyme, and subsequently formed normal extrinsic ocular or jaw muscles. In these muscles it was evident that only the myogenic populations were derived from grafted trunk cells. Ancillary findings were that grafted trunk paraxial mesoderm frequently interfered with the movement of neural crest cells which form the corneal posterior epithelial and stromal tissues, and that some grafted cells formed ectopic intramembranous bones adjacent to the eye. These results verify that presumptive connective tissue-forming mesenchyme derived from the neural crest imparts spatial patterning information upon myogenic cells that invade it. Moreover, interactions between myotomal cells and both lateral plate somatic mesoderm in the trunk and neural crest mesenchyme in the head appear to operate according to similar mechanisms.     

An Intermediate in the evolution of superfast sonic muscles

Background

Intermediate forms in the evolution of new adaptations such as transitions from water to land and the evolution of flight are often poorly understood. Similarly, the evolution of superfast sonic muscles in fishes, often considered the fastest muscles in vertebrates, has been a mystery because slow bladder movement does not generate sound. Slow muscles that stretch the swimbladder and then produce sound during recoil have recently been discovered in ophidiiform fishes. Here we describe the disturbance call (produced when fish are held) and sonic mechanism in an unrelated perciform pearl perch (Glaucosomatidae) that represents an intermediate condition in the evolution of super-fast sonic muscles.

Results

The pearl perch disturbance call is a two-part sound produced by a fast sonic muscle that rapidly stretches the bladder and an antagonistic tendon-smooth muscle combination (part 1) causing the tendon and bladder to snap back (part 2) generating a higher-frequency and greater-amplitude pulse. The smooth muscle is confirmed by electron microscopy and protein analysis. To our knowledge smooth muscle attachment to a tendon is unknown in animals.

Conclusion

The pearl perch, an advanced perciform teleost unrelated to ophidiiform fishes, uses a slow type mechanism to produce the major portion of the sound pulse during recoil, but the swimbladder is stretched by a fast muscle. Similarities between the two unrelated lineages, suggest independent and convergent evolution of sonic muscles and indicate intermediate forms in the evolution of superfast muscles.     

An experimental study of craniofacial growth in a heterotopic rat head transplant

In order to examine whether or not facial bones are themselves able to regulate their own growth, we devised a new experimental model in which we transplanted the whole head of an infant rat to the body of an isohistogeneic adult rat by means of microvascular anastomoses. The advantage of this model is that the transplanted head has neither scars nor any moving soft tissues that could modify growth around facial bones. Using this model, we conducted a study of the nasomaxillary region that has led us to conclude that facial bones do in fact regulate their own growth. The results also suggested that facial bone sutures play a more active role in the growth process than presently suspected.     

Pax 6: mastering eye morphogenesis and eye evolution.

Pax 6 genes from various animal phyla are capable of inducing ectopic eye development, indicating that Pax 6 is a master control gene for eye morphogenesis. It is proposed that the various eye-types found in metazoa are derived from a common prototype, monophyletically, by a mechanism called intercalary evolution.     

Divergent decapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis

In the fruit fly Drosophila, the patterning genes decapentaplegic and wingless contribute to the spatial control of retina development in an antagonistic manner. We examined the expression patterns of these genes in the developing visual system of the hemimetabolous grasshopper Schistocerca americana and the primitive holometabolous beetle species Tribolium castaneum. The pattern of wingless expression was strongly conserved as a pair of lateral domains at the anterior margins of both the developing retina and the developing optic lobes. The expression of decapentaplegic, on the other hand, is different. Unlike in Drosophila, no decapentaplegic expression was detected before the onset of photoreceptor differentiation in the retinal precursor tissue of either grasshopper or beetle. Moreover, the subsequent expression of decapentaplegic in the latter species was not concentrated in the moving front of retina differentiation, as in Drosophila, but observed in anterior and posterior regions. Our results indicate that Drosophila eye development contains elements of both ancestral and derived regulatory gene functions. The requirement for decapentaplegic as an antagonist of wingless during the early development of the Drosophila retina might have originated during the evolution of insect metamorphosis.     

Cephalic muscles of Cyclostomes (hagfishes and lampreys) and Chondrichthyes (sharks,rays and holocephalans): comparative anatomy and early evolution of the vertebrate head muscles

Living vertebrate diversity comprises hagfishes and lampreys (Cyclostomata), elasmobranchs and holocephalans (Chondrichthyes), and bony fish which include tetrapods (Osteichthyes). Based on dissections and an extensive comparative analysis, we provide an updated overview of the anatomy, homologies and evolution of cyclostome and chondrichthyan cephalic muscles, with osteichthyans as primary comparative taxa. The analysis also infers plesiomorphic conditions for vertebrates and gnathostomes. We follow a uniform myological terminology for the Gnathostomata to demonstrate that the last common ancestor of extant vertebrates probably had a single intermandibularis and other mandibular muscles (labial muscles), some constrictores hyoidei and branchiales, and epibranchial and hypobranchial muscle sheets. The division of the cucullaris into levatores arcuum branchialium and protractor pectoralis is an osteichthyan synapomorphy and reflects an evolutionary trend towards a greater separation between the head and pectoral girdle that culminated in the formation of the tetrapod neck. Hence, this paper addresses a long‐standing, central issue regarding vertebrate comparative anatomy. It thus provides a valuable basis for future evolutionary, developmental and functional studies of vertebrates and/or of specific vertebrate subgroups/model organisms. © 2014 The Linnean Society of London     

Genetics of craniofacial development and malformation

The head is anatomically the most sophisticated part of the body and its evolution was fundamental to the origin of vertebrates; understanding its development is a formidable problem in biology. A synthesis of embryology, evolution and mouse genetics is shaping our understanding of head development and in this review we discuss its application to studies of human craniofacial malformations. Many of these disorders have their origins in specific embryological processes, including abnormalities of brain patterning, of the migration and fusion of tissues in the face, and of bone differentiation in the skull vault.