The Platyhelminthes are located in an important position with respect to the evolution of metazoan . 3 They are widely recognized as being among the simplest organisms possessing three tissue layers (triploblasts), bilateral symmetry, cephalization, and complex organ systems. Planarians have characteristic organs along the anteroposterior axis, such as a pair of eyes and auricles, and a brain with simple architecture in the anterior head. One of the most notable characteristics of planarians is their high regenerative ability. They can regenerate whole animals, including a functional brain, from tiny fragments from almost any part of their bodies after amputation. An early worker on planarians described them as “almost immortal under the edge of the knife”. Later, Charles Darwin, famous as the author of The Origin of Species, was also interested in the regenerative ability of planarians. The robust regenerative abilities of planarians are based on a population of pluripotent stem cells called neoblasts, which are the only mitotic somatic cells in adults and are distributed throughout the body in planarians.
Structural and Cellular Aspects of the Planarian Brain
In addition to planarian regenerative ability, they possess another important biological feature; that is, planarians belong to an evolutionarily early group that acquired a central nervous system (CNS). The planarian CNS is composed of two morphologically distinct structures: a bilobed brain, composed of about 2.0– 3.0 10^4 neurons in an adult planarian of about 8 mm in length, with nine branches on each outer side in the anterior region of the animal, and two longitudinal ventral nerve cords (VNCs) along the body (Fig. 4.1b). The brain is composed of a cortex of nerve cells in its outer region and a core of nerve fibers in its inner region (Fig. 4.2a). A pair of eyes is located on the dorsal side at the level of the third lateral branch of the brain. These morphological features of the brain structure suggested that external stimuli sensed by various organs, and the information thus acquired
by sensory neurons, might be accumulated inside the brain, and then processed and integrated to transduce the signals into the activity of motor neurons.
Flatworms are the earliest known animals to have a brain, and the simplest animals alive to have bilateral symmetry. They are also the simplest animals with organs that form from three germ layers. 1
THE URBILATERIAN BRAIN REVISITED: NOVEL INSIGHTS INTO OLD QUESTIONS FROM NEW FLATWORM CLADES 2
Flatworms are classically considered to represent the simplest organizational form of all living bilaterians with a true central nervous system. Based on their simple body plans, all flatworms have been traditionally grouped together in a single phylum at the base of the bilaterians. Current molecular phylogenomic studies now split the flatworms into two widely separated clades, the acoelomorph flatworms and the platyhelminth flatworms, such that the last common ancestor of both clades corresponds to the urbilaterian ancestor of all bilaterian animals. Remarkably, recent comparative neuroanatomical analyses of acoelomorphs and platyhelminths show that both of these flatworm groups have complex anterior brains with surprisingly similar basic neuroarchitectures. Taken together, these findings imply that fundamental neuroanatomical features of the brain in the two separate flatworm groups are likely to be primitive and derived from the urbilaterian brain.
CONSERVED DEVELOPMENTAL PROGRAMS FOR DIVERSE BILATERIAN BRAINS
At the structural level, the brains of higher deuterostomes such as vertebrates and higher protostomes such as arthropods or annelids are strikingly different. Moreover the embryological processes that give rise to these brains are also different in these two animal groups. The brain and dorsally located nerve cord of vertebrates derive from a dorsal neuroectoderm that invaginates to form a neural tube. In contrast, the brain and ventrally located ganglionic nerve cord of arthropods and annelids derive from a ventral neuroectoderm. In addition, the mechanism of neural progenitor proliferation shows significant differences. As shown for several arthropod taxa, but also probably true for other protostome phyla, asymmetrically dividing neural stem cells (neuroblasts) generate morphologically distinct lineages of neurons/glial cells which also form structural units of the brain. By contrast, neural progenitors in vertebrates form a layer of symmetrically dividing cells. These cells eventually switch to asymmetric divisions when producing neurons, but no evidence exists to date that neurons descending from individual progenitors form structural units, such as individual brainstem nuclei, or cortical layers. These and other differences in CNS structure and development have been used as one basis for the classification of “vertebrate-like” notoneuralia versus “invertebrate-like” gastroneuralia types. It is interesting to ask what the CNS of the common bilaterian ancestor looked like, and how one can envisage the evolutionary changes that led to the divergence of the two types of nervous systems.
Key developmental processes such as regionalization of the neural primordium and specification of certain cell types are conserved in brain development of protostomes and deuterostomes. This implies that the brains of all bilaterian animals are evolutionarily related and derive from an ancestral urbilaterian ancestor which may have already possessed a developmental genetic program for brain architecture of considerable complexity.
Classically, flatworms are considered to have the simplest organization of all bilaterians which is characterized by a lack of coelom, respiratory system, circulatory system, skeletal system, and through-gut. Flatworms have been traditionally grouped together in a single phylum, the members of which are thought to have been least changed from the ancestral bilaterian form. Accordingly, many traditional phylogenies placed this classical platyhelminth monophylum in a group of “acoelomates” at a basal position in the bilaterian tree. Given this phylogenetic perspective, the flatworm brain might also be least changed from the ancestral form and hence most representative of the urbilaterian brain. This notion is in accordance with classical comparative neuroanatomical studies that considered flatworms to be the most primitive bilaterians possessing a true central nervous system.
With a look towards earlier evolutionary stages, i.e., to the medusa or polyp-like ancestor of flatworms, it was suggested that the orthogon derives from the diffuse nerve net whereby concentrations of neurons at certain places (e.g., around the mouth or tentacles, coalesce into coherent fiber tracts; looking forward towards “higher animals”, it was hypothesized that a further concentration and restriction of neural elements had ensued, in such a way that in the ancestors of protostomes the dorsal tracts of the orthogon were eliminated, and in the ancestors of chordates the ventral ones.
With the advent of molecular phylogenetics a decade ago, a major revision of the classical bilaterian phylogeny became necessary. In this revision, the entire platyhelminth phylum was removed from its basal position and firmly embedded within the lophotrochozoans, one of the two protostome superclades (Fig. 2B). As a result, the platyhelminth flatworms could no longer be considered to be more basal than any of the other lophotrochozoan phyla such as the annelids or molluscs. From this revised phylogenetic point of view there is no a priori reason to assume that the flatworm CNS should manifest primitive features characteristic of the urbilaterian brain. Indeed based on this revised phylogeny none of the living animals would correspond to intermediates between protostomes and deuterostomes, hence, making it more difficult to reconstruct the anatomical organization of the ancestral bilaterian brain from any extant species.
Recent neuroanatomical studies demonstrate that both types of flatworms have relatively complex anterior brains that consist of a cortex of neural cell bodies and a central neuropile with numerous commissural and longitudinal fiber bundles. Early classical histological analyses of the central nervous systems of acoelomorph flatworms reported the presence of a bilobed central brain composed of numerous neuronal cell bodies associated with complex commissural and connective fiber bundles
3. Brain Evolution by Design, Shuichi Shigeno Yasunori Murakami Tadashi Nomura, page 82