TY - JOUR
T1 - Neurogenesis in directly and indirectly developing enteropneusts
T2 - of nets and cords
AU - Kaul-Strehlow, Sabrina
AU - Urata, Makoto
AU - Minokawa, Takuya
AU - Stach, Thomas
AU - Wanninger, Andreas
N1 - Funding Information:
We thank the staff of the Research Center for Marine Biology Tohoku University in Asamushi, Japan. This study was funded by a Lise-Meitner grant from the Austrian Science Fund (FWF) to SK-S (M 1485-B19). The collection trip of SK-S to Japan was financially supported by a stipend from the Research Center for Marine Biology, Tohoku University Japan. Dr. Elena S. Casey (Georgetown University) is thanked for provision of material of S. kowalevskii. Dr. Alen Kristof (University Vienna) and Dr. Thomas Schwaha (University Vienna) are thanked for technical guidance with the confocal microscope. We thank Julia Bauder (University Vienna) and Barbara Schädl (University Vienna) for additional sectioning of B. misakiensis.
Publisher Copyright:
© 2015, The Author(s).
PY - 2015/6/6
Y1 - 2015/6/6
N2 - 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.
AB - 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.
KW - Bipolar receptor cell
KW - Deuterostome
KW - Enteropneusts
KW - Evolution
KW - Hemichordates
KW - Nervous system
KW - Neurogenesis
KW - Plexus
KW - Serotonin
UR - http://www.scopus.com/inward/record.url?scp=84930414450&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84930414450&partnerID=8YFLogxK
U2 - 10.1007/s13127-015-0201-2
DO - 10.1007/s13127-015-0201-2
M3 - Article
AN - SCOPUS:84930414450
SN - 1439-6092
VL - 15
SP - 405
EP - 422
JO - Organisms Diversity and Evolution
JF - Organisms Diversity and Evolution
IS - 2
ER -