Figure 3 - uploaded by Mario Pestarino
Content may be subject to copyright.
Schematic drawing showing the anatomical organization of the lancelet. White arrows show the direction of water current, and black arrows indicate the route of food particles. a, anus; at, atriopore; d, mid-gut diverticulum; fe, frontal eye complex; fp, food particles; he, Hesse eyecups; i, intestine; ir, ilio-colon ring; mg, mid-gut; n, notochord; nt, neural tube; ph, pharynx; r, rostrum (modified from Ruppert & Barnes 1994).
Source publication
Serotonin (5-hydroxytryptamine) is a biogenic amine distributed throughout the metazoans and has an old evolutionary history. It is involved as a developmental signal in the early morphogenesis of both invertebrates and vertebrates, whereas in adults it acts mainly as a neurotransmitter and gastrointestinal hormone. In vertebrates, serotonin regula...
Contexts in source publication
Context 1
... dorsal sensory branch, innervating the dorsolateral por- tion of the skin, contains serotonin and gives rise to collaterals innervating skin sensory cells or ending encapsulated ( Figure 2G,H). In 2-day larvae, endocrine-like cells containing sero- tonin are visible for the first time exclusively at the level of the ilio-colon ring of the gut in the ventral position ( Figure 3B,C). No immunoreactivity was detected in eggs, zygotes and blastulae. ...
Context 2
... immunoreactivity was confined to the central ner- vous system (CNS) and digestive tract in adult specimens of B. floridae ( Figure 3). A dorsolateral group of serotonin- containing nerve cell bodies were found in the roof of the cerebral vesicle, posterior to the frontal eye complex and anterior to the Joseph cells. ...
Citations
... Similarly, in the larva of Microcosmus vulgaris (Pyuridae) 5-HT was found in a few cells close to the gravity sensing otolith (De Bernardi et al., 2006). In Phallusia mammillata swimming larvae, 5-HT was detected in the sensory vesicle, adhesive papillae, epidermal trunk neurons, and epidermal tail neurons (Pennati et al., 2001) while in the larvae of Botrylloides leachi (Aplousobranchia), 5-HT signal was observed only in peripheral neurons of the papillae . ...
... In adults of Ciona, 5-HT containing cells were reported in the pharyngeal bands, in the esophagus and in the stomach; some of them were also aligned in a band extending from the peripharyngeal band of the branchial basket to the endostyle (Braun and Stach, 2016). In juvenile of P. mammillata, 5-HT-positive cells were found in the peripharyngeal band, in the gut and two bilaterally symmetric rows of cells between bands 7 and 8 of the endostyle (Pennati et al., 2001). This area also contains cells capable of fixing iodine (Nilsson et al., 1988) and calcitonin-like cells (Thorndyke and Probert, 1979). ...
... Based on the detailed morphological description provided by Burighel and Milanesi, the serotonergic cells described in the digestive system of ascidians may be identified as endocrine cells (Burighel and Milanesi, 1975), and considered homolog to the vertebrate enterochromaffin cells (Gershon, 2004). 5-HT-positive cells are also present in the enteric system of cephalochordates (Candiani et al., 2001) but not in hemichordates or echinoderms (Strano et al., 2019;Mercurio et al., 2019b), suggesting that enteric 5-HT may be a novel feature of chordate evolution. ...
Serotonin (5 hydroxytryptamine, 5-HT) is a biogenic amine of ancient origin that is widespread among animals. It plays multiple roles during development and in adults as neurotransmitter at synaptic level and neuro hormone controlling complex behaviors in both vertebrates and invertebrates. Tunicates occupy a key phylogenetic position to understand the evolution of serotonin functions since they are the sister group of vertebrates. The presence of serotonin in tunicates was first reported in adults of the ascidian Ciona robusta (formerly Ciona intestinalis) in the 1946. Since then, serotonin systems have been in many tunicate species and its functions during embryogenesis and metamorphosis explored. We reviewed the current knowledge about serotonin in these animals first by comparing its presence and localization in larvae and adults of different species. Then, we focused on the model organism Ciona for which data regarding sequences and expression patterns of genes involved in serotonin synthesis and function have been reported. Overall, we provided a comprehensive overview of serotonergic machinery in tunicates and gave hints for future studies in this field.
... Serotonin modulates the maturation of oocytes and sperm in the reproductive system of vertebrates and invertebrates [55][56][57]. Serotonin is found in oocytes of invertebrates [58][59][60][61] and vertebrates [62][63][64]. In L. stagnalis, an increase in the intracellular content of serotonin in the early stages of embryogenesis causes morphological and behavioural changes in young individuals [21,40]. ...
Intense species-specific locomotion changes the behavioural and cognitive states of various vertebrates and invertebrates. However, whether and how reproductive behaviour is affected by previous increased motor activity remains largely unknown. We addressed this question using a model organism, the pond snail Lymnaea stagnalis. Intense crawling in shallow water for two hours had previously been shown to affect orienting behaviour in a new environment as well as the state of the serotonergic system in L. stagnalis. We found that the same behaviour resulted in an increased number of egg clutches and the total number of eggs laid in the following 24 h. However, the number of eggs per clutch was not affected. This effect was significantly stronger from January to May, in contrast to the September-December period. Transcripts of the egg-laying prohormone gene and the tryptophan hydroxylase gene, which codes for the rate-limiting enzyme in serotonin synthesis, were significantly higher in the central nervous system of snails that rested in clean water for two hours after intense crawling. Additionally, the neurons of the left (but not the right) caudo-dorsal cluster (CDC), which produce the ovulation hormone and play a key role in oviposition, responded to stimulation with a higher number of spikes, although there were no differences in their resting membrane potentials. We speculate that the left-right asymmetry of the response was due to the asymmetric (right) location of the male reproductive neurons having an antagonistic influence on the female hormonal system in the hermaphrodite mollusc. Serotonin, which is known to enhance oviposition in L. stagnalis, had no direct effect on the membrane potential or electrical activity of CDC neurons. Our data suggest that (i) two-hour crawling in shallow water enhances oviposition in L. stagnalis, (ii) the effect depends on the season, and (iii) the underlying mechanisms may include increased excitability of the CDC neurons and increased expression of the egg-laying prohormone gene.
... Similar to bacteria and protozoa, transmitter substances such as 5-HT, catecholamines, ACh, and GABA in protozoans only have been detected in the cells of early embryos of all species studied (see [6,[96][97][98][99][100][101][102][103][104]). ...
In 1921, Otto Loewi published his report that ushered in the era of chemical transmission of biological signals. January 2021 marked the 90th anniversary of the birth of Professor Gennady A. Buznikov, who was the first to study the functions of transmitters in embryogenesis. A year earlier it was 60 years since his first publication in this field. These data are a venerable occasion for a review of current knowledge on the mechanisms related to classical transmitters such as 5-hydroxytryptamine, acetylcholine, catecholamines, etc., in animals lacking neural elements and prenervous invertebrate embryos.
... The late 1950s/early 1960s saw the fi rst observations that various monoamines and other low molecular weight substances operating in the adult body as neurotransmitters are present at the early developmental stages, long before the formation of the nervous system [Numanoi, 1955;Buzinkov and Manukhin, 1961]. Further studies showed that serotonin is present in oocytes and the dividing embryos of animals of extreme systematic diversity: polychetes [Emanuelsson, 1974], nemertea [Buznikov et al., 1964], nudibranch mollusks [Buznikov et al., 2003], cephalochordates [Candiani et al., 2001], echinoderms and bony fi sh [Buznikov et al., 1964], amphibia [Fukumoto et al., 2005;Beyer et al., 2012;Nikishin et al., 2012], birds [Emanuelsson et al., 1988], and mammals [Basu et al., 2008]. Experimental studies demonstrated that monoamines are involved in regulating a wide spectrum of processes in the preneural stages of development in very diverse animals (for review see [Buznikov et al., 2001;Buznikov, 2007]). ...
A significant number of integrative functions in the body are mediated by the monoaminergic systems: a set of low molecular weight transmitters which are biogenic amines (serotonin and dopamine), the enzymes of their metabolism, and their receptors. This makes monoamines a major component of the nervous and endocrine systems in the body, determining the adaptogenic capabilities of the body in continually changing environmental conditions. Using our own experimental material as an example, along with published data, we discuss the regulatory role of monoamines in development, starting with the oocyte and early cleavage stage and extending to formation of the neural networks underlying behavior. The classical ligand-receptor mechanism is considered, along with the mechanism of noncanonical modification of intracellular proteins (monoaminylation) and their contribution to adaptive regulation at different stages of development. The role of monoamines as a conservative factor binding environmental signals and the physiology of the developing body is discussed.
... floridae), serotonin has been first detected at neurula stage in the forming neural tube . Later in 2/3-day old larva, it has been found in two populations of cells, one in the cerebral vesicle including frontal eye complex, and another in the inner epithelium of the gut ( Figure 1B and Table 2A) (Holland and Holland, 1993;Candiani et al., 2001;Vopalensky et al., 2012). In 6-day old larvae, the rostral serotonin-positive cells differentiate into dorsal serotonergic neurons and are segmentally repeated along the spinal cord . ...
We review the occurrence of biogenic amines and their potential role as neurotransmitters in the nervous system of three groups of invertebrate deuterostomes: tunicates, cephalochordates, and echinoderms. In addition to an overview of biogenic amines in each subphylum, we focus on a few species, including the sea squirts Ciona intestinalis, C. robusta, C. savignyi, and Phallusia mammillata (tunicates), the lancelets Branchiostoma lanceolatum and Branchiostoma floridae (cephalochordates), and the sea urchin Strongylocentrotus purpuratus (echinoderms). We chose these species as they are the most studied invertebrate deuterostomes in the field of evolutionary developmental biology (EvoDevo). Providing a comparative picture of the expression and role of neurotransmitters in deuterostomes will contribute to understanding the evolution of these neural signaling systems. Such an approach represents a new frontier of comparative neuroanatomy and neurobiology, and a prerequisite to uncover the homology of neuronal structures and circuits in deuterostomes with such diverse body plan organization and complexity.
... Serotonin-lir in the brain of adult specimens: (0) absent; (1) present. Serotonin-lir in the brain has been detected only in investigated outgroup species (Baumgarten et al., 1973;Sakharov and Salimova, 1980;Holland and Holland, 1993;Candiani et al., 2001;Barreiro-Iglesias et al., 2009), Salpida, Doliolida (Braun and Stach, 2018) and O. fusiformis (Stach, 2005), but could not be detected in other tunicate species examined. 88. ...
... The gastrointestinal tract is the part of the intestinal tract posterior to the esophagus. Serotonin-lir cells are located in the gastrointestinal tract of T. democratica, ascidians, and species belonging to the outgroup (Sakharov and Salimova, 1980;Candiani et al., 2001;Barreiro-Iglesias et al., 2009;Stach, 2016, 2018;Figs 12e,f,i,j,n and 13a,b,e,i-k,n). ...
With approximately 3000 marine species, Tunicata represents the most disparate subtaxon of Chordata. Molecular phylogenetic studies support Tunicata as sister taxon to Craniota, rendering it pivotal to understanding craniate evolution. Although successively more molecular data have become available to resolve internal tunicate phylogenetic relationships, phenotypic data have not been utilized consistently. Herein these shortcomings are addressed by cladistically analyzing 117 phenotypic characters for 49 tunicate species comprising all higher tunicate taxa, and five craniate and cephalochordate outgroup species. In addition, a combined analysis of the phenotypic characters with 18S rDNA ‐sequence data is performed in 32 OTU s. The analysis of the combined data is congruent with published molecular analyses. Successively up‐weighting phenotypic characters indicates that phenotypic data contribute disproportionally more to the resulting phylogenetic hypothesis. The strict consensus tree from the analysis of the phenotypic characters as well as the single most parsimonious tree found in the analysis of the combined dataset recover monophyletic Appendicularia as sister taxon to the remaining tunicate taxa. Thus, both datasets support the hypothesis that the last common ancestor of Tunicata was free‐living and that ascidian sessility is a derived trait within Tunicata. “Thaliacea” is found to be paraphyletic with Pyrosomatida as sister taxon to monophyletic Ascidiacea and the relationship between Doliolida and Salpida is unresolved in the analysis of morphological characters; however, the analysis of the combined data reconstructs Thaliacea as monophyletic nested within paraphyletic “Ascidiacea”. Therefore, both datasets differ in the interpretation of the evolution of the complex holoplanktonic life history of thaliacean taxa. According to the phenotypic data, this evolution occurred in the plankton, whereas from the combined dataset a secondary transition into the plankton from a sessile ascidian is inferred. Besides these major differences, both analyses are in accord on many phylogenetic groupings, although both phylogenetic reconstructions invoke a high degree of homoplasy. In conclusion, this study represents the first serious attempt to utilize the potential phylogenetic information present in phenotypic characters to elucidate the inter‐relationships of this diverse marine taxon in a consistent cladistic framework.
... Serotonin-lir in the brain of adult specimens: (0) absent; (1) present. Serotonin-lir in the brain has been detected only in investigated outgroup species (Baumgarten et al., 1973;Sakharov and Salimova, 1980;Holland and Holland, 1993;Candiani et al., 2001;Barreiro-Iglesias et al., 2009), Salpida, Doliolida (Braun and Stach, 2018) and O. fusiformis (Stach, 2005), but could not be detected in other tunicate species examined. 88. ...
... The gastrointestinal tract is the part of the intestinal tract posterior to the esophagus. Serotonin-lir cells are located in the gastrointestinal tract of T. democratica, ascidians, and species belonging to the outgroup (Sakharov and Salimova, 1980;Candiani et al., 2001;Barreiro-Iglesias et al., 2009;Stach, 2016, 2018;Figs 12e,f,i,j,n and 13a,b,e,i-k,n). ...
With approximately 3000 marine species, Tunicata represents the most disparate subtaxon of Chordata. Molecular phylogenetic studies support Tunicata as sister taxon to Craniota, rendering it pivotal to understanding craniate evolution. Although successively more molecular data have become available to resolve internal tunicate phylogenetic relationships, phenotypic data have not been utilized consistently. Herein these shortcomings are addressed by cladistically analyzing 117 phenotypic characters for 49 tunicate species comprising all higher tunicate taxa, and five craniate and cephalochordate outgroup species. In addition, a combined analysis of the phenotypic characters with 18S rDNA‐sequence data is performed in 32 OTUs. The analysis of the combined data is congruent with published molecular analyses. Successively up‐weighting phenotypic characters indicates that phenotypic data contribute disproportionally more to the resulting phylogenetic hypothesis. The strict consensus tree from the analysis of the phenotypic characters as well as the single most parsimonious tree found in the analysis of the combined dataset recover monophyletic Appendicularia as sister taxon to the remaining tunicate taxa. Thus, both datasets support the hypothesis that the last common ancestor of Tunicata was free‐living and that ascidian sessility is a derived trait within Tunicata. “Thaliacea” is found to be paraphyletic with Pyrosomatida as sister taxon to monophyletic Ascidiacea and the relationship between Doliolida and Salpida is unresolved in the analysis of morphological characters; however, the analysis of the combined data reconstructs Thaliacea as monophyletic nested within paraphyletic “Ascidiacea”. Therefore, both datasets differ in the interpretation of the evolution of the complex holoplanktonic life history of thaliacean taxa. According to the phenotypic data, this evolution occurred in the plankton, whereas from the combined dataset a secondary transition into the plankton from a sessile ascidian is inferred. Besides these major differences, both analyses are in accord on many phylogenetic groupings, although both phylogenetic reconstructions invoke a high degree of homoplasy. In conclusion, this study represents the first serious attempt to utilize the potential phylogenetic information present in phenotypic characters to elucidate the inter‐relationships of this diverse marine taxon in a consistent cladistic framework.
... Indeed, following the specification of the ANE, the subsequent differentiation of this neuroectodermal territory into a brain or an apical organ has been shown to be mediated by a similar core set of neurogenic transcription factors that include Six3, FoxQ2, Rx, and FoxG (Yankura et al. 2010;Holland et al. 2013;Range 2014). Moreover, at the cellular level, both chordate brains and ambulacrarian apical organs contain clusters of serotonergic neurons, which are characterized by neurites projecting posteriorly (Candiani et al. 2001;Byrne et al. 2007;Stach 2014). Thus, based on these conserved features, chordate brains and ambulacrarian apical organs have frequently been described as being evolutionarily related (Wei et al. 2009;Tosches and Arendt 2013;Arendt et al. 2016). ...
The evolutionary origin and history of metazoan nervous systems has been at the heart of numerous scientific debates for well over a century. This has been a particularly difficult issue to resolve within the deuterostomes, chiefly due to the distinct neural architectures observed within this group of animals. Indeed, deuterosomes feature central nervous systems, apical organs, nerve cords, and basiepidermal nerve nets. Comparative analyses investigating the anatomy and molecular composition of deuterostome nervous systems have nonetheless succeeded in identifying a number of shared and derived features. These analyses have led to the elaboration of diverse theories about the origin and evolutionary history of deuterostome nervous systems. Here, we provide an overview of these distinct theories. Further, we argue that deciphering the adult nervous systems of representatives of all deuterostome phyla, including echinoderms, which have long been neglected in this type of surveys, will ultimately provide answers to the questions concerning the ancestry and evolution of deuterostome nervous systems.
... In order to come to a better understanding of chordate evolution, a strategy could be to reconstruct ground patterns of the taxa to be compared in detail (Stach 2015;Scholtz 2013;Richter and Wirkner 2014). The more than 2500 described species of tunicates offer the opportunity to do so, because they comprise a bewildering variety of life cycles, encompassing the sessile ascidians as well as the free-living, planktonic salps, the brightly bioluminescent pyrosomes, the doliolids with their unique polymorphism, and the larvaceans with their intricate and elaborate filtering houses (e.g., Bone 1998;Lemaire 2011). Molecular phylogenetic studies of the relationships of higher taxonomic groups within Tunicata are highly contradictory (see e.g. ...
As one of the three major chordate taxa, the highly diverse taxon, Tunicata has always played a key role in considerations of evolutionary origins of vertebrates, especially since several larger-scaled molecular phylogenetic analyses support the hypothesis that tunicates are the sister group to vertebrates. Molecular phylogenetic studies of the relationships within Tunicata are highly contradictory, and cladistic analyses of morphological characters for Tunicata remained limited. In order to come to a better understanding of chordate evolution, we comparatively investigated nine different tunicate species belonging to five different higher tunicate taxa: Phlebobranchiata, Aplousobranchiata, Stolidobranchiata, Thaliacea, and Appendicularia using immunofluorescence labeling with antibodies against serotonin in conjunction with confocal laser scanning microscopy. We found that adult ascidians are comparable in regard to their respective patterns of serotonin-like immunoreactive (serotonin-lir) cells, whereas the planktonic tunicates differ in several aspects. The distribution patterns of serotonin-lir cells in tunicates suggest that serotonin-like immunoreactivity can behave as an independent character during evolution. While the distribution pattern of serotonin-lir cells agrees well with classical taxonomic groupings, phylogenetic interpretation remains inconclusive, as ad hoc hypotheses are always necessary to explain contradictory character distribution. Based on light-microscopically observed morphology, we could distinguish three different types of serotonin-lir cells, most probably functionally distinctive. These were approximately spherical serotonin-lir cells, possibly involved in the control of ciliary beating and mucus secretion, elongated serotonin-lir cells potentially involved in hormonal regulation of feeding, and serotonin-lir neurons that might be implicated in the initiation of locomotory behavior.
... e application of modern microscopical techniques such as immunohistochemistry, in combination with confocal laser-scanning microscopy, has improved our understanding of neural development in amphioxus (e.g. Yasui et al. 1998, Yasui and Kaji 2008, Yasui et al. 2014, Candiani et al. 2001), but much remains to be done. Breeding populations of amphioxus can now be maintained in the laboratory (Li et al. 2013for B. belcheri, Benito-Gutierrez et al. 2013for B. lanceolatum, and Yasui et al. 2013 for B. japonicum, with work in progress on B. oridae), which will free researchers from the constraints of seasonal spawning. ...
For many biologists the nervous system is a particularly fascinating organ system. The nervous system is involved in or is even responsible for many features that are regarded as being characteristic of animals in general. Since the last comprehensive work was published about 50 years ago, the time has probably come to provide a new review on recent, newly gathered knowledge on the structure of invertebrate nervous systems, especially since new methods have come into use. These advances now enable us to demonstrate neuronal architecture down to the level of the genes and the cell types involved, allowing a new view on nervous systems and comparisons among different taxa. These new findings may help in development of new hypotheses, or support of existing hypotheses on phylogenetic relationships and evolutionary pathways in the nervous system. In spite of many open questions we already have a good knowledge of how nervous systems work, how they are constructed, and how they may have evolved. There is certain evidence that the first nervous systems are represented by rather simple sensory–motor circuits, followed by nerve nets (plexus) located within the epithelia, and finally neuronal circuits composed of sensory cells, interneurons, and brains. Therefore, this book concentrates on invertebrates and structure and these new evolutionary aspects, here discussed as ‘research highlights’ or ‘perspectives’. Sensory structures are only touched on peripherally. Whereas some taxa have been studied extensively and well-written reviews may already exist, in other taxa our knowledge on the nervous system is still scant and scarce.
