Evolutionary Developmental Studies of the Vertebrate Body Plan and its Origins


Our research focuses on how the diverse spectrum of exquisite morphological patterns exhibited by the animal body came to be. By comparing various embryos and gene expressions, it is only possible to seek out commonalities of pattern, leading to the identification of homologous elements or generalized body plans, which are not so different per se from the concept of "unity of types" initially proposed by Geoffroy St. Hilaire. We believe that the inability to make straightforward comparisons can in fact be more meaningful at times, as this permits us to explore the developmental changes that resulted in the acquisition of non-comparable novelties. Such phenomena suggest a loss of developmental constraints, which may have led to creation of new connections, new patterns, and new cell-cell interactions, thereby allowing the acquisition of de novo expression domains for developmental regulatory genes that may be responsible for specific patterning events. Such changes are theoretically obtained by heterotopic and heterochronic shifts in developmental programs, as first suggested by Haeckel. Comparative methods thus potentially provide a way to understand the developmental and mechanical backgrounds for evolutionary novelties that more or less involve the cooption of gene regulatory networks. Comparative morphology and embryology are thus our primary strategy for gaining a better understanding of the nature of the fundamental questions and obtaining hints about ways to arrive at the answers. These hints can be found everywhere, not only under the microscope, but also in museums and libraries.


 1. Kopfproblem
Goethe suggested that the vertebrate skull is composed of several vertebrae; Oken went even farther and said that we are nothing but a vertebral column. The theory of head segmentation was denied by Thomas Huxley, but was resurrected in the form of a comparative embryological problem, and today, our group addresses the same problem from Evo-Devo perspectives. This "head problem" is central to our understanding of the vertebrate body plan and its evolutionary origins. Major questions include:

    i. What are the 'head cavities' initially recognized in elasmobranch embryos? Are they present in cyclostomes? How are they similar to trunk somites?

   ii. If the vertebrate head mesoderm is somehow unique, how is it related to the rostral mesodermal elements in amphioxus? Is it possible to establish homologies between amphioxus rostral segments and any of the head mesodermal domains in vertebrates?

   iii. What was the sequence of events or changes introduced into the developmental programs of vertebrate ancestors, in the transition from non-vertebrate to vertebrate body plan?

In addition to lampreys, hagfish, shark, and some model vertebrates, in 2011 we began working with amphioxus to help tackle this problem.

 2. Jaw and early vertebrate evolution
  Possession of a biting jaw characterizes most of the modern vertebrates (crown gnathostomes), as opposed to the jawless vertebrates, which include only two groups of animals: lampreys and hagfish. These animals are collectively referred to as "cyclostomes," as their oral apparatus does not consist of dorsoventrally articulated jaw elements. In modern molecular phylogeny, it has been suggested that they form a monophyletic clade. However, there still remain unsolved questions as to this relationship since the anatomy of the two cyclostomes are conspicuously different. To obtain insight into the evolutionary and developmental background of jaw acquisition, we have to speculate on the ancestral condition of cyclostomes to evaluate the truly derived nature of the developmental patterns and processes of gnathostome mandibular arch, for which embryological studies of hagfish are necessary.
  Until recently, hagfish embryos had been unavailable for more than a century since Bashford Dean described the external morphology of a complete developmental series of Bdellostoma stouti. In 2007, a postdoc in our lab at the time, Kinya (Ginjiro) Ota, succeeded in obtaining fertilized eggs from the adult Eptatretus burgeri, making it possible to study the development of hagfish with modern technologies. So far, we have shown that this animal show early embryonic developmental patterns and gene expressions surprisingly similar to lampreys and gnathostomes, consistent with the evolutionary position of this animal suggested by recent molecular phylogeny. We are now comparing their morphological developmental patterns with those of gnathostome and lamprey embryos.

 3. Vertebrate 'Neck' as a transitional domain between head and trunk
The vertebrate neck represents the most enigmatic part of the body, as it is located at the interface between the somitomeric trunk and branchiomeric head. In this region, somites and postotic pharyngeal arches arise at the same axial levels, and therefore this region develops both somitomeric spinal nerves, such as the hypoglossal, and branchiomeric cranial nerves, such as the glossopharyngeal and vagus. Simultaneously, the neural crest cells arising from this domain can follow both the trunk-specific and head-specific migratory pathways to prefigure the morphology of the peripheral nerves. Thus, many of the structures are classified into cephalic- and trunk-like elements. To which category then should we assign the accessory nerve? Or the cucullaris muscle? Apparently, these elements possess both trunk- and head-like traits. These elements are also not found in cyclostomes. It is very likely, therefore, that these elements may represent new patterns based on a new developmental program that was secondarily acquired in gnathostome lineage. And this evolutionary novelty is apparently associated with the shoulder girdle and pectoral fin. Since the pectoral fin-like process is already found in some basal (jawless) gnathostomes, it may be more appropriate to think that the event was connected to the obtainment of the shoulder girdle. If so, how was this achieved? Recent findings suggest that development of the cucullaris muscles may be more complicated than has been realized. The same would therefore also be true for the accessory nerves. In various model- and non-model vertebrate embryos, we are currently observing developmental patterning of the accessory nerve to understand this gnathostome-specific trait.

  4. Turtle shells
The turtle anatomy is unusual since its ribs, the anlage of the carapace, develop in a superficial layer and cover the entire shoulder girdle. Their morphology potentially represents a typical case of heterotopy, involving the repatterning of mesodermal derivatives.
  We have isolated a number of developmental regulatory genes specifically activated in an embryonic structure in the turtle, the carapacial ridge (CR), which has been regarded as a novelty to induce carapacial patterning. The repertoire of the CR-expressed genes was suggestive of activation of the Wnt-HGF signalling pathways, associated with, and responsible for, the growth of the CR. There were no comparable patterns of these genes' expressions in the chicken embryo. Thus, this phenomenon appears to represent a novel, turtle-specific form of regulation; however, we have not yet identified when and how this co-opted network could be activated in the early development of turtle embryos. We are now investigating this mechanism using a whole-genomic and epigenetic approaches.

 5. Ontogeny and phylogeny
It is also within the scope of our research to seek to understand the relationships between developmental and evolutionary processes. In Irie and Kuratani (2011), we have shown that vertebrate embryos follow hourglass-like divergence during embryogenesis, exhibiting a phylotype-like stage at pharyngular stages. Such a conserved stage of development (Haupttyp) has been recognized since von Baer (1828), and our recent understanding is that this is the stage where the basic vertebrate body plan appears. This, however, does not exclusively rule out Haeckel-like recapitulation. Namely, after the appearance of the vertebrate phylotype, a more restricted similarity may arise among closely related species, representing the common developmental pattern of more restricted taxa, such as amniotes and mammals.