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Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords.

Kaul-Strehlow S, Urata M, Minokawa T, Stach T, Wanninger A - Org. Divers. Evol. (2015)

Bottom Line: We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells.Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring.Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Zoology, University of Vienna, Althanstr. 14, 1090 Vienna, Austria.

ABSTRACT

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.

No MeSH data available.


Related in: MedlinePlus

Phylogenetic relationships of major metazoan taxa compiled from recent molecular analyses (i.e., Hejnol et al. 2009; Philippe et al. 2011). Schematic representation of the adult nervous system is included for each taxon. For more information, see text
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Fig1: Phylogenetic relationships of major metazoan taxa compiled from recent molecular analyses (i.e., Hejnol et al. 2009; Philippe et al. 2011). Schematic representation of the adult nervous system is included for each taxon. For more information, see text

Mentions: Numerous comparative studies on the nervous system have revealed highly variable neural anatomies in multicellular animals, ranging from a simple nerve net in cnidarians to highly complex central nervous systems (CNS) in vertebrates (Nieuwenhuys et al. 1998) and some protostomes (e.g., arthropods and cephalopods) (Bullock and Horridge 1965; Nixon and Young 2003; Strausfeld 2012). In Ambulacraria, a group of nonchordate deuterostomes that include echinoderms, pterobranchs, enteropneusts, and arguably xenacoelomorphs (Philippe et al. 2011), the nervous system of most of them comprises both a basiepidermal plexus as well as centralized portions (Fig. 1) (Bullock 1946; Cavey and Märkel 1994; Chia and Koss 1994; Knight-Jones 1952; Stach et al. 2012). It is still debated whether a plexus-like nervous system or a concentrated CNS was present in the last common ancestor of deuterostomes (LCAD). On the one hand, molecular analyses of the enteropneust Saccoglossus kowalevskii show circumferential expression of neuro-patterning genes throughout the entire ectoderm (Lowe et al. 2003; Pani et al. 2012; Cunningham and Casey 2014), thus supporting the presence of a basiepidermal plexus in the LCAD (Holland 2003; Gerhart et al. 2005). On the other hand, similarities in the anteroposterior and mediolateral patterning including presence and position of specific neuronal types between the ventral CNS of some protostomes (annelids and arthropods) and the dorsal CNS of chordates lead some authors to propose a CNS in the LCAD (Denes et al. 2007; Arendt et al. 2008; Nomaksteinsky et al. 2009; Holland et al. 2013; Miyamoto and Wada 2013). Both contradicting hypotheses are mainly based on molecular genetic analyses, whereas potentially informative neuro-anatomical data has barely been integrated. And, this is because data on neural morphogenesis in juvenile enteropneusts still remain scarce (e.g., Kaul and Stach 2010; Miyamoto et al. 2010) and precise anatomical descriptions of the nervous system are mainly based on histological analyses of adult specimens (Bullock 1946; Knight-Jones 1952).Fig. 1


Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords.

Kaul-Strehlow S, Urata M, Minokawa T, Stach T, Wanninger A - Org. Divers. Evol. (2015)

Phylogenetic relationships of major metazoan taxa compiled from recent molecular analyses (i.e., Hejnol et al. 2009; Philippe et al. 2011). Schematic representation of the adult nervous system is included for each taxon. For more information, see text
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4514687&req=5

Fig1: Phylogenetic relationships of major metazoan taxa compiled from recent molecular analyses (i.e., Hejnol et al. 2009; Philippe et al. 2011). Schematic representation of the adult nervous system is included for each taxon. For more information, see text
Mentions: Numerous comparative studies on the nervous system have revealed highly variable neural anatomies in multicellular animals, ranging from a simple nerve net in cnidarians to highly complex central nervous systems (CNS) in vertebrates (Nieuwenhuys et al. 1998) and some protostomes (e.g., arthropods and cephalopods) (Bullock and Horridge 1965; Nixon and Young 2003; Strausfeld 2012). In Ambulacraria, a group of nonchordate deuterostomes that include echinoderms, pterobranchs, enteropneusts, and arguably xenacoelomorphs (Philippe et al. 2011), the nervous system of most of them comprises both a basiepidermal plexus as well as centralized portions (Fig. 1) (Bullock 1946; Cavey and Märkel 1994; Chia and Koss 1994; Knight-Jones 1952; Stach et al. 2012). It is still debated whether a plexus-like nervous system or a concentrated CNS was present in the last common ancestor of deuterostomes (LCAD). On the one hand, molecular analyses of the enteropneust Saccoglossus kowalevskii show circumferential expression of neuro-patterning genes throughout the entire ectoderm (Lowe et al. 2003; Pani et al. 2012; Cunningham and Casey 2014), thus supporting the presence of a basiepidermal plexus in the LCAD (Holland 2003; Gerhart et al. 2005). On the other hand, similarities in the anteroposterior and mediolateral patterning including presence and position of specific neuronal types between the ventral CNS of some protostomes (annelids and arthropods) and the dorsal CNS of chordates lead some authors to propose a CNS in the LCAD (Denes et al. 2007; Arendt et al. 2008; Nomaksteinsky et al. 2009; Holland et al. 2013; Miyamoto and Wada 2013). Both contradicting hypotheses are mainly based on molecular genetic analyses, whereas potentially informative neuro-anatomical data has barely been integrated. And, this is because data on neural morphogenesis in juvenile enteropneusts still remain scarce (e.g., Kaul and Stach 2010; Miyamoto et al. 2010) and precise anatomical descriptions of the nervous system are mainly based on histological analyses of adult specimens (Bullock 1946; Knight-Jones 1952).Fig. 1

Bottom Line: We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells.Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring.Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Zoology, University of Vienna, Althanstr. 14, 1090 Vienna, Austria.

ABSTRACT

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.

No MeSH data available.


Related in: MedlinePlus