The evolution of anural larvae in molgulid ascidians

Ascidians are urochordates, marine invertebrates with non-feeding motile chordate tadpole larvae, except in the family Molgulidae. Urodele, or tailed, Molgulids have typical ascidian chordate tadpole larvae possessing tails with muscle cells, a notochord, and a dorsal hollow nerve cord. In contrast, anural (or tail-less) Molgulids lack a tail and defining chordate features. Molecular phylogenies generated with 18S and 28S ribosomal sequences indicate that Molgulid species fall into at least four distinct clades, three of which have multiple anural members. This refined and expanded phylogeny allows careful examination of the factors that may have influenced the evolution of tail-less ascidians.     

Evolution of alternate modes of development in ascidians.

Ascidians have evolved alternate modes of development in which the conventional tadpole larva is remodeled or eliminated. Adultation, the precocious development of adult features in the larval head, is caused by superimposing the larval and adult differentiation programs. Caudalization, the addition of muscle cells to the larval tail, is caused by enhancing muscle induction or increasing the number of muscle cell divisions before terminal differentiation. Adultation and caudalization are correlated with increased egg size, suggesting dependence on maternal processes. Anural development, the elimination of the larval stage, is caused by maternal and zygotic events resulting in abbreviation and deletion of larval developmental programs. An example of a maternal change in anural species is the modification of the egg cytoskeleton during oogenesis, whereas a zygotic change may involve altered cell interactions during embryogenesis. Interspecific hybridization experiments suggest that some aspects of anural development may be caused by loss-of-function mutations. The dissociation of developmental programs is a key process in changing the mode of development in ascidians.     

Larval adhesive organs and metamorphosis in ascidians

Summary The cup-shaped adhesive papillae of Distaplia occidentalis evert at the onset of metamorphosis and each transforms into a hyperboloidal configuration. The rate of transformation is a function of temperature. At 14° C complete eversion takes about 30 seconds. Myoepithelial cells that extend from the rim to the base on the cup contract. Simultaneously the central part of the papilla advances 60–70 m. During the last phases of eversion, collocytes (cells that secrete adhesives) on the inner wall of the cup and on the sides of the axial protrusion flow outward and form a collar-like structure.The myoepithelial cells contain arrays of thick and thin filaments. These become compacted during contraction. The surfaces of these cells become extensively folded as they shorten to about 1/3 of rest length. According to the proposed model the myoepithelial cells are the driving force in papillary eversion.Immediately after eversion is completed the papillae begin to retract. Eversion of the papillae is not inhibited by cytochalasin B, but the process of retraction is reversibly inhibited.Some histological characteristics of five types of everting papillae in four families of ascidians are compared.     

Larval adhesive organs and metamorphosis in ascidians

Summary The larva of Distaplia occidentalis bears three cup-shaped adhesive papillae, each with a prominent axial protrusion. At the onset of metamorphosis these organs rapidly evert through fenestrations in the cuticular layers of tunic exposing hyaline caps of adhesive. Additional adhesive material is secreted from collocytes during eversion. The stickiness of the papillae facilitates attachment to a variety of substrates.Each papilla is composed of more than 900 cells; six different types were identified. The wall of the cup contains about 260 myoepithelial cells with long attenuated processes. These extend from the rim of the cup to the base in the parietal (inner) layer. The apices of the myoepithelial cells are held in place by 11 pairs of specialized anchor cells bearing long bulbous microvilli. When the myoepithelial cells contract they force the axial protrusion forward and transform the papilla into a hyperboloidal configuration. The papilla is innervated by small motor fibers, but sensory fibers were not detected. The adhesive papillae of Distaplia are discussed in relationship to nine other recognizable types of papillae in the ascidians.     

Evolution of the brain and sensory organs in Sphenisciformes: new data from the stem penguin Paraptenodytes antarcticus

Penguins have undergone dramatic changes associated with the evolution of underwater flight and subsequent loss of aerial flight, which are manifest and well documented in the musculoskeletal system and integument. Significant modification of neurosensory systems and endocranial spaces may also be expected along this locomotor transition. However, no investigations of the brain and sensory organs of extinct stem lineage Sphenisciformes have been carried out, and few data exist even for extant species of Spheniscidae. In order to explore neuroanatomical evolution in penguins, we generated virtual endocasts for the early Miocene stem penguin Paraptenodytes antarcticus, three extant penguin species (Pygoscelis antarctica, Aptenodytes patagonicus, Spheniscus magellanicus), and two outgroup species (the common loon Gavia immer and the Laysan albatross Phoebastria immutabilis). These endocasts yield new anatomical data and phylogenetically informative characters from the brain, carotid arteries, pneumatic recesses, and semicircular canal system. Despite having undergone over 60 million years of evolution since the loss of flight, penguins retain many attributes traditionally linked to flight. Features associated with visual acuity and proprioception, such as the sagittal eminence and flocculus, show a similar degree of development to those of volant birds in the three extant penguins and Paraptenodytes antarcticus. These features, although clearly not flight‐related in penguins, are consistent with the neurological demands associated with rapid manoeuvring in complex aquatic environments. Semicircular canal orientation in penguins is similar to volant birds. Interestingly, canal radius is grossly enlarged in the fossil taxon Pa. antarcticus compared to living penguins and outgroups. In contrast to all other living birds, the contralateral anterior tympanic recesses of extant penguins do not communicate. An interaural pathway connecting these recesses is retained in Pa. antarcticus, suggesting that stem penguins may still have employed this connection, potentially to enhance directional localization of sound. Paedomorphosis, already identified as a potential factor in crown clade penguin skeletal morphology, may also be implicated in the failure of an interaural pathway to form during ontogeny in extant penguins. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166 , 202–219.     

Evolution of cerebral vesicles and their sensory organs in an ascidian larva

Sorrentino M., Manni L., Lane N. J. and Burighel P. 2000. Evolution of cerebral vesicles and their sensory organs in an ascidian larva. —Acta Zoologica (Stockholm) 81 : 243–258 The ascidian larval nervous system consists of the brain (comprising the visceral ganglion and the sensory vesicle), and, continuous with it, a caudal nerve cord. In most species two organs, a statocyst and an ocellus with ciliary photoreceptors, are contained in the sensory vesicle. A third presumptive sensory organ was sometimes found in an ‘auxiliary’ ganglionic vesicle. The development and morphology of the sensory and auxiliary ganglionic vesicles in Botryllus schlosseri and their associated organs was studied. The sensory vesicle contains a unique organ, the photolith, responding to both gravity and light. It consists of a unicellular statocyst, in the form of an expanded pigment cup receiving six photoreceptor cell extensions. Presumptive mechano‐receptor cells (S1 cells), send ciliary and microvillar protrusions to contact the pigment cup. A second group of distinctive cells (S2), slightly dorsal to the S1 cells, have characteristic microvillar extensions, resembling photoreceptor. We concur with the idea that the photolith is new and derived from a primitive statocyst and the S2 cells are the remnant of a primitive ocellus. In the ganglionic vesicle some cells contain modified cilia and microvillar extensions, which resemble the photoreceptor endings of the photolith. Our results are discussed in the light of two possible scenarios regarding the evolution of the nervous system of protochordates.     

Chiton integument: development of sensory organs in juvenile Mopalia muscosa

The girdle epidermis of adult Mopalia muscosa secretes several types of structures, including calcareous spicules and innervated hairs. Newly metamorphosed chitons superficially resemble adult animals, but they lack the adult girdle ornaments, shell sculpture, and coloration. The morphogenesis of the adult girdle structures has not been described previously for any species. Juvenile Mopalia muscosa secrete hairs at metamorphosis, but it was not known if these hairs were sensory or if they were retained as the animals grew. I discovered that the hairs of juveniles become the tips of adult hairs. When juvenile hairs are detectable by light microscopy the sensory components already exist, suggesting that they are functional receptor organs. The other girdle ornaments of young juveniles, the primary calcareous spicules, are lost as the animal grows. I also demonstrated that the hairs are not uniquely innervated; the same sensory structures are produced in conjunction with other girdle ornaments on the marginal and ventral faces.     

Different vascular permeability between the sensory and secretory circumventricular organs of adult mouse brain

The blood-brain barrier (BBB) prevents free access of circulating molecules to the brain and maintains a specialized brain environment to protect the brain from blood-derived bioactive and toxic molecules; however, the circumventricular organs (CVOs) have fenestrated vasculature. The fenestrated vasculature in the sensory CVOs, including the organum vasculosum of lamina terminalis (OVLT), subfornical organ (SFO) and area postrema (AP), allows neurons and astrocytes to sense a variety of plasma molecules and convey their information into other brain regions and the vasculature in the secretory CVOs, including median eminence (ME) and neurohypophysis (NH), permits neuronal terminals to secrete many peptides into the blood stream. The present study showed that vascular permeability of low-molecular-mass tracers such as fluorescein isothiocyanate (FITC) and Evans Blue was higher in the secretory CVOs and kidney as compared with that in the sensory CVOs. On the other hand, vascular permeability of high-molecular-mass tracers such as FITC-labeled bovine serum albumin and Dextran 70,000 was lower in the CVOs as compared with that in the kidney. Prominent vascular permeability of low- and high-molecular-mass tracers was also observed in the arcuate nucleus. These data demonstrate that vascular permeability for low-molecular-mass molecules is higher in the secretory CVOs as compared with that in the sensory CVOs, possibly for large secretion of peptides to the blood stream. Moreover, vascular permeability for high-molecular-mass tracers in the CVOs is smaller than that of the kidney, indicating that the CVOs are not totally without a BBB.     

Evolution of Emx genes and brain development in vertebrates.

Emx1 and Emx2 genes are known to be involved in mammalian forebrain development. In order to investigate the evolution of the Emx gene family in vertebrates, a phylogenetic analysis was carried out on the Emx genes sequenced in man, mice, frogs, coelacanths and zebrafish. The results demonstrated the existence of two clades (Emx1 and Emx2), each grouping one of the two genes of the investigated taxa. The only exception was the zebrafish Emx1-like gene which turned out to be a sister group to both the Emx1 and Emx2 clusters. Such striking sequence divergence observed for the zebrafish Emx1-like gene could indicate that it is not orthologous to the other Emx1 genes, and therefore, in vertebrates there must be three Emx genes. Alternatively, if the zebrafish emx1 gene is orthologous to the tetrapod one, it must have undergone to strong diversifying selection.     

Comparative studies on the structure of reproductive organs of four botryllid ascidians

Reproductive organs of four botryllid ascidians, Botryllus primigenus, Botryllus schlosseri, Botrylloides violaceus and Botrylloides leachi, were studied histologically. In every species, the egg follicle consisting of an egg and its inner and outer follicles, is attached to the follicle stalk, the vesicle being composed of a flat epithelium, which in its turn is connected to the atrial epithelium or to the brood pouch specialized from it. In B. schlosseri, the egg is ovulated into the atrial cavity and remains there held by the brood cup, of which the inner epithelium is derived from the follicle stalk and the outer one from the atrial epithelium. In B. primigenus, the brood pouch develops as a diverticulum of the atrial cavity, around the entrance of which a fold differentiates from the atrial epithelium and closes the pouch during embryogenesis. In both species of Botrylloides, the brood pouch is formed by the outgrowth of the thickened atrial epithelium into the blood space, the entrance of which is closed during embryogenesis. The discarded outer follicle completely disintegrates soon after ovulation in B. schlosseri, but part of it remains throughout embryogenesis in the blood space in B. primigenus or projecting into the interior of the brood pouch in Botrylloides. In primigenus, the testis, when it accompanies the egg follicle, is placed at the bottom of the brood pouch and the sperm is shed through the pouch prior to ovulation. In B. schlosseri and the Botrylloides species, the testis is located independently from the egg follicle and the sperm matures after ovulation.     

The development of the sensory organs of the legs in the blowfly,Phormia regina

Summary The development of the sensory neurons of the legs of the blowfly,Phormia regina has been described from the third instar larva to the late pupa using immunohistochemical staining. The leg discs of the third instar larva contain 8 neurons of which 5 come to lie in the fifth tarsomere of the developing leg. Whereas 2 neurons persist at least to the late pupa, the other cells degenerate. The first neurons of gustatory sensilla arise in the fifth tarsomere at about 1.5 h after formation of the puparium. Most of these sensilla, however, appear within a short time period beginning at about 18 h. The femoral chordotonal sensory neurons first appear at the time of formation of the puparium, as a mass of cells situated in the distal femur. During later pupal development 2 groups of these cells come to lie at the femur-trochanter border, where they become the proximal femoral chordotonal organ of the adult; the remaining cells become the distal femoral chordotonal organ. Other scolopidial neurons appear later in development. The nerve pathways of the late pupal leg are established either by the axons of the cells that are present in the larval leg disc or by new outgrowing processes of sensory neurons. In the tibia, the initial direction of new outgrowth differs in different regions of the segment: proximal tibial neurons grow distally, while distal tibial neurons grow initially proximally.     

Evolution of sensory systems

Sensory systems evolve and enable organisms to perceive their sensory Umwelt, the unique set of cues relevant for their survival. The multiple components that comprise sensory systems — the receptors, cells, organs, and dedicated high-order circuits — can vary greatly across species. Sensory receptor gene families can expand and contract across lineages, resulting in enormous sensory diversity. Comparative studies of sensory receptor function have uncovered the molecular basis of receptor properties and identified novel sensory receptor classes and noncanonical sensory strategies. Phylogenetically informed comparisons of sensory systems across multiple species can pinpoint when sensory changes evolve and highlight the role of contingency in sensory system evolution.     

Molecular evidence from ascidians for the evolutionary origin of vertebrate cranial sensory placodes

Cranial sensory placodes are specialised areas of the head ectoderm of vertebrate embryos that contribute to the formation of the cranial sense organs and associated ganglia. Placodes are often considered a vertebrate innovation, and their evolution has been hypothesised as one key adaptation underlying the evolution of active predation by primitive vertebrates. Here, we review recent molecular evidence pertinent to understanding the evolutionary origin of placodes. The development of vertebrate placodes is regulated by numerous genes, including members of the Pax, Six, Eya, Fox, Phox, Neurogenin and Pou gene families. In the sea squirt Ciona intestinalis (a basal chordate and close relative of the vertebrates), orthologues of these genes are deployed in the development of the oral and atrial siphons, structures used for filter feeding by the sessile adult. Our interpretation of these findings is that vertebrate placodes and sea squirt siphon primordia have evolved from the same patches of specialised ectoderm present in the common ancestor of the chordates.     

Mitosis and body patterning during morphallactic development of palleal buds in ascidians

Spatiotemporal distribution of mitosis and anteroposterior body patterning during morphallactic development of palleal buds in the ascidian, Polyandrocarpa misakiensis, have been studied histologically in the presence or absence of 1.5 mM colchicine. Local cell division became evident at the proximal end of the inner, atrial epithelium of 1.5-day intact buds. This and other histological evidence showed that the primary cell activation took place at that region. In 2-day intact buds, mitotic activity spread out from the proximal end toward the lateral epithelial wall that had the lower (more anterior) positional information, referred to as the secondary cell activation. These primary and secondary activation sites were the presumptive domains of the gut and pharyngeal rudiments which specified the anteroposterior body pattern of a bud. Surgical manipulations to induce the reversal of bud polarity caused the conversion of the secondary activation site and of the pharyngeal domain, but had no effect on the primary cell activation. Thus, positional information in ascidians contributes to the formation of the pharynx by specifying the secodary cell activation site. On the other hand, a large discontinuity in positional information enhanced the primary cell activity. When two positional information gaps were constructed in a single bud, the primary cell activation occurred at two sites, resulting in an additional gut rudiment. The results of this study are discussed in the context of the possible basic mechanism that the budding in ascidians shares with epimorphic fields.