scholarly journals Early embryogenesis and organogenesis in the annelid Owenia fusiformis

2021 ◽  
Author(s):  
Allan Martín Carrillo-Baltodano ◽  
Océane Seudre ◽  
Kero Guynes ◽  
José María Martín-Durán
Keyword(s):  
Nervous System ◽  
Sister Group ◽  
Early Embryogenesis ◽  
Apical Organ ◽  
Diverse Group ◽  
Spiral Cleavage ◽  
Early Cleavage ◽  
Apical Tuft ◽  
Evolution And Development ◽  
Active Proliferation

AbstractBackgroundAnnelids are a diverse group of segmented worms within Spiralia, whose embryos exhibit spiral cleavage and a variety of larval forms. While most modern embryological studies focus on species with unequal spiral cleavage nested in Pleistoannelida (Sedentaria + Errantia), a few recent studies looked into Owenia fusiformis, a member of the sister group to all remaining annelids and thus a key lineage to understand annelid and spiralian evolution and development. However, the timing of early cleavage and detailed morphogenetic events leading to the formation of the idiosyncratic mitraria larva of O. fusiformis remain largely unexplored.ResultsO. fusiformis undergoes equal spiral cleavage where the first quartet of animal micromeres are slightly larger than the vegetal macromeres. Cleavage results in a coeloblastula approximately five hours post fertilization (hpf) at 19 °C. Gastrulation occurs via invagination and completes four hours later, with putative mesodermal precursors and the chaetoblasts appearing 10 hpf at the dorsoposterior side. Soon after, at 11 hpf, the apical tuft emerges, followed by the first neurons (as revealed by the expression of elav1 and synaptotagmin1) in the apical organ and the prototroch by 13 hpf. Muscles connecting the chaetal sac to various larval tissues develop around 18 hpf and by the time the mitraria is fully formed at 22 hpf, there are FMRFamide+ neurons in the apical organ and prototroch, the latter forming a prototrochal ring. As the mitraria feeds, it grows in size and the prototroch expands through active proliferation. The larva becomes competent after ∼3 weeks post fertilization at 15 °C, when a conspicuous juvenile rudiment has formed ventrally.ConclusionsO. fusiformis embryogenesis is similar to that of other equal spiral cleaving annelids, supporting that equal cleavage is associated with the formation of a coeloblastula, gastrulation via invagination, and a feeding trochophore-like larva in Annelida. The nervous system of the mitraria larva forms earlier and is more complex than previously recognised and develops from anterior to posterior, which is likely an ancestral condition to Annelida. Altogether, our study identifies the major developmental events during O. fusiformis ontogeny, defining a conceptual framework for future investigations.

scholarly journals Early Embryogenesis and Organogenesis in the Annelid Owenia Fusiformis

2021 ◽  
Author(s):  
Allan Martín Carrillo-Baltodano ◽  
Océane Seudre ◽  
Kero Guynes ◽  
Jose M Martin-Duran
Keyword(s):  
Nervous System ◽  
Sister Group ◽  
Early Embryogenesis ◽  
Apical Organ ◽  
Diverse Group ◽  
Spiral Cleavage ◽  
Early Cleavage ◽  
Apical Tuft ◽  
Evolution And Development ◽  
Active Proliferation

Abstract Background : Annelids are a diverse group of segmented worms within Spiralia, whose embryos exhibit spiral cleavage and a variety of larval forms. While most modern embryological studies focus on species with unequal spiral cleavage nested in Pleistoannelida (Sedentaria + Errantia), a few recent studies looked into Owenia fusiformis , a member of the sister group to all remaining annelids and thus a key lineage to understand annelid and spiralian evolution and development. However, the timing of early cleavage and detailed morphogenetic events leading to the formation of the idiosyncratic mitraria larva of O. fusiformis remain largely unexplored.Results : O. fusiformis undergoes equal spiral cleavage where the first quartet of animal micromeres are slightly larger than the vegetal macromeres. Cleavage results in a coeloblastula approximately five hours post fertilization (hpf) at 19 ºC. Gastrulation occurs via invagination and completes four hours later, with putative mesodermal precursors and the chaetoblasts appearing 10 hpf at the dorsoposterior side. Soon after, at 11 hpf, the apical tuft emerges, followed by the first neurons (as revealed by the expression of elav1 and synaptotagmin1 ) in the apical organ and the prototroch by 13 hpf. Muscles connecting the chaetal sac to various larval tissues develop around 18 hpf and by the time the mitraria is fully formed at 22 hpf, there are FMRFamide + neurons in the apical organ and prototroch, the latter forming a prototrochal ring. As the mitraria feeds, it grows in size and the prototroch expands through active proliferation. The larva becomes competent after ~3 weeks post fertilization at 15 ºC, when a conspicuous juvenile rudiment has formed ventrally.Conclusions : O. fusiformis embryogenesis is similar to that of other equal spiral cleaving annelids, supporting that equal cleavage is associated with the formation of a coeloblastula, gastrulation via invagination, and a feeding trochophore-like larva in Annelida. The nervous system of the mitraria larva forms earlier and is more complex than previously recognized and develops from anterior to posterior, which is likely an ancestral condition to Annelida. Altogether, our study identifies the major developmental events during O. fusiformis ontogeny, defining a conceptual framework for future investigations.

scholarly journals Early embryogenesis and organogenesis in the annelid Owenia fusiformis

EvoDevo ◽  
2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Allan Martín Carrillo-Baltodano ◽  
Océane Seudre ◽  
Kero Guynes ◽  
José María Martín-Durán
Keyword(s):  
Sister Group ◽  
Early Embryogenesis ◽  
Apical Organ ◽  
Diverse Group ◽  
Spiral Cleavage ◽  
Early Cleavage ◽  
Apical Tuft ◽  
Evolution And Development ◽  
Synaptotagmin 1 ◽  
Active Proliferation

Abstract Background Annelids are a diverse group of segmented worms within Spiralia, whose embryos exhibit spiral cleavage and a variety of larval forms. While most modern embryological studies focus on species with unequal spiral cleavage nested in Pleistoannelida (Sedentaria + Errantia), a few recent studies looked into Owenia fusiformis, a member of the sister group to all remaining annelids and thus a key lineage to understand annelid and spiralian evolution and development. However, the timing of early cleavage and detailed morphogenetic events leading to the formation of the idiosyncratic mitraria larva of O. fusiformis remain largely unexplored. Results Owenia fusiformis undergoes equal spiral cleavage where the first quartet of animal micromeres are slightly larger than the vegetal macromeres. Cleavage results in a coeloblastula approximately 5 h post-fertilization (hpf) at 19 °C. Gastrulation occurs via invagination and completes 4 h later, with putative mesodermal precursors and the chaetoblasts appearing 10 hpf at the dorso-posterior side. Soon after, at 11 hpf, the apical tuft emerges, followed by the first neurons (as revealed by the expression of elav1 and synaptotagmin-1) in the apical organ and the prototroch by 13 hpf. Muscles connecting the chaetal sac to various larval tissues develop around 18 hpf and by the time the mitraria is fully formed at 22 hpf, there are FMRFamide+ neurons in the apical organ and prototroch, the latter forming a prototrochal ring. As the mitraria feeds, it grows in size and the prototroch expands through active proliferation. The larva becomes competent after ~ 3 weeks post-fertilization at 15 °C, when a conspicuous juvenile rudiment has formed ventrally. Conclusions Owenia fusiformis embryogenesis is similar to that of other equal spiral cleaving annelids, supporting that equal cleavage is associated with the formation of a coeloblastula, gastrulation via invagination, and a feeding trochophore-like larva in Annelida. The nervous system of the mitraria larva forms earlier and is more elaborated than previously recognized and develops from anterior to posterior, which is likely an ancestral condition to Annelida. Altogether, our study identifies the major developmental events during O. fusiformis ontogeny, defining a conceptual framework for future investigations.

The Larval Apical Organ in the Holothuroid Chiridota gigas (Apodida): Inferences on Evolution of the Ambulacrarian Larval Nervous System

2006 ◽  
Vol 211 (2) ◽  
pp. 95-100 ◽  
Author(s):  
Maria Byrne ◽  
Mary A. Sewell ◽  
Paulina Selvakumaraswamy ◽  
Thomas A. A. Prowse
Keyword(s):  
Nervous System ◽  
Apical Organ ◽  
Larval Nervous System

scholarly journals Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms

2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Yongxin Li ◽  
Akihito Omori ◽  
Rachel L. Flores ◽  
Sheri Satterfield ◽  
Christine Nguyen ◽  
...  
Keyword(s):  
Genetic Basis ◽  
Developmental Stages ◽  
Sister Group ◽  
Body Plan ◽  
The Body ◽  
Last Common Ancestor ◽  
Evolution And Development ◽  
Gene Sets ◽  
Green Sea Urchin ◽  
Feather Star

AbstractEchinoderms are an exceptional group of bilaterians that develop pentameral adult symmetry from a bilaterally symmetric larva. However, the genetic basis in evolution and development of this unique transformation remains to be clarified. Here we report newly sequenced genomes, developmental transcriptomes, and proteomes of diverse echinoderms including the green sea urchin (L. variegatus), a sea cucumber (A. japonicus), and with particular emphasis on a sister group of the earliest-diverged echinoderms, the feather star (A. japonica). We learned that the last common ancestor of echinoderms retained a well-organized Hox cluster reminiscent of the hemichordate, and had gene sets involved in endoskeleton development. Further, unlike in other animal groups, the most conserved developmental stages were not at the body plan establishing phase, and genes normally involved in bilaterality appear to function in pentameric axis development. These results enhance our understanding of the divergence of protostomes and deuterostomes almost 500 Mya.

scholarly journals Ossicle development of the crinoid Florometra serratissima through larval stages

2017 ◽  
Vol 95 (3) ◽  
pp. 183-192 ◽  
Author(s):  
Ariane Comeau ◽  
Cory D. Bishop ◽  
Christopher B. Cameron
Keyword(s):  
Electron Microscopy ◽  
Scanning Electron Microscopy ◽  
Soft Tissues ◽  
Sister Group ◽  
Coralline Algae ◽  
Rapid Radiation ◽  
Larval Stages ◽  
Evolution And Development ◽  
Feather Star ◽  
Scanning Electron

Crinoids are the oldest living class of echinoderm and sister group to the remaining eleutherozoan clade and so are key to discussions on the evolution and development of the echinoderm skeleton. Here we present the intraspecific variation of ossicle development of the feather star Florometra serratissima (A.H. Clark, 1907) during its three larval stages: doliolaria, cystidean, and early pentacrinoid. To induce settlement, larvae were cultured on a sea table in glass bowls containing coralline algae. The soft tissues of 60 larvae were dissolved to isolate and to observe the ossicles with compound microscopy and scanning electron microscopy. From the late doliolaria stage to 56-day-old pentacrinoids, a total of four types of ossicle developed: oral plates, basal plates, columnar stalk ossicles, and an attachment disk. Occasionally, an additional plate was found under the basal plates, which may represent a vestigial infrabasal plate. The shape of the attachment disk was plastic to accommodate the substrate. Crinoid ossicle development is variable in size, shape, and number, and the timing of development is asynchronous; traits that may have contributed to the early rapid radiation and phenotypic disparity of echinoderms.

Structure and organization of the nervous system in the actinotroch larva of Phoronis vancouverensis

1990 ◽  
Vol 327 (1244) ◽  
pp. 655-685 ◽  
Keyword(s):  
Nervous System ◽  
Nerve Cell ◽  
Central Element ◽  
Neuromuscular Control ◽  
The Body ◽  
Oral Feeding ◽  
Apical Organ ◽  
Morphological Evidence ◽  
Ciliary Band ◽  
Phylogenetic Implications

The nervous system of the earliest functional stage of the actinotroch larva of Phoronis vancouverensis is described based on ultrastructural surveys and three-dimensional reconstructions, including serial reconstructions of selected parts of the system. The central element and main source of fibres in the system is the apical organ. Nerve cell bodies were found here and in the surrounding apical epithelium, but nowhere else in the body. Given the limitations of the methods used, the presence of nerve cell bodies elsewhere in the body cannot be ruled out, but based on this work and a recent study by A. Hay-Schmidt of whole larvae, it seems unlikely they occur in any numbers. The larval nervous system is thus highly centralized, an advanced and rather specialized feature in comparison with some other larval types, specifically those of primitive spiralia and echinoderms, in which nerve cell bodies are more widely distributed in the larval epithelium. The largest single nerve in the body is the primary hood nerve, which runs around the pre-oral hood slightly back from its margin. The nerve is a compact, well-defined tract of approximately 40 fibres, with an investment of glial-like accessory cells. A second set of smaller, accessory nerves run parallel to the primary nerve between it and the hood margin. The hood nerves all join at the base of the hood on either side of the mouth to form a pair of adoral nerve centres. A number of small nerves cross the hood from the apical organ to the hood nerves. Three of these are large enough to be considered major nerves: one is medial and connects to the centre of the hood margin, the other two are dorsolateral and connect to the adoral nerve centres. Fibre tracings, which show the distribution of vesicle-filled terminals and varicosities, suggest the hood nerves are mainly involved in neuromuscular control, specifically, in lifting the hood. This involves the stimulation, in sequence, of the radial and circular hood muscles by the primary and accessory hood nerves, respectively. Cells at the hood margin are organized somewhat in the fashion of a conventional ciliary band, but there is no obvious morphological evidence that any of the hood nerves are involved in neurociliary control. A diffuse plexus of small nerves connects the above apical structures to the nerves supplying the tentacles. There are two main tentacle nerves, the primary tentacle nerve, which runs along the upper, oral margin of the tentacular ciliary band, and a smaller accessory nerve, which arises as a branch from the primary nerve, and runs along the lower, aboral margin of the band. There is also a row of uniciliate sensory receptor cells at the oral margin of the band. Each cell has a basal process ending in a vesicle-filled terminal that abuts fibres in the upper tentacle nerve, and forms junctions with them. The cells themselves produce no other fibres. They appear to be mechanosensory, and are probably involved in initiating the hood lift response, which can be triggered by touching the top surface of the tentacles. Additional large, vesicle-filled terminals branch from the fibres in the primary tentacle nerve. Their positions suggest a neurociliary function. The accessory tentacle nerve is associated mainly with muscle cells. A series of small nerves, which probably arise as branches from the larger tentacle nerves, supply the region below the tentacles, later the site of the telotroch. The comparative and phylogenetic implications of the above are discussed. Phoronids are generally interpreted as being intermediate between deuterostomes and protostomes, with a curious mixture of characteristics of both groups. Phoronids are probably only distantly related to spiralian protostomes, but they are, strictly speaking, protostomes, and their larvae resemble the trochophore-type larvae of spiralia in many respects. Regarding ciliary band substructure and patterns of innervation, the actinotroch possesses too few features that are clearly primitive to support a detailed comparison with spiralian larvae, but the pre-oral hood band shows a sufficient number of prototroch-like features, to suggest the hood band and prototroch could be homologous. There is evidence for parallel evolution, in the two groups, of an increasingly centralized nervous system that provides improved effector control via nerve cells located in and around the apical organ. No evidence was obtained to support suggested homologies between the post-oral band of the actinotroch and circumoral or post-oral feeding bands in deuterostome larvae. The two appear, in fact, to be quite dissimilar in terms of their innervation. The results thus support conventional interpretations of the relationship between phoronids and other major groups.

Sign in / Sign up

Export Citation Format

Share Document