A single origin of animal excretory organs

Gąsiorowski, Ludwik; Andrikou, Carmen; Bump, Paul; Janßen, Ralf; Budd, Graham E.; Lowe, Christopher J.; Hejnol, Andreas

doi:10.1101/2020.11.15.378034

Cited by 3 publications

(3 citation statements)

References 55 publications

(123 reference statements)

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“…7c–h, 8b–d,f–g), a pair of eyes appear near the apical tuft (Helm et al, 2016; Wilson, 1932) and the nephridia enlarge on both left and right sides of the hyposphere (Fig. 7c,e,g) (Gąsiorowski et al, 2020; Smith et al, 1987; Wilson, 1932). As previously described (Helm et al, 2016; Helm et al, 2017), the nervous system also becomes more complex, with new nerves (peripheral nerves 1–3 and dorsal nerve) connecting the apical organ to various regions of the prototroch, and the circumesophageal connectives to the juvenile nerve cord (Fig.…”

Section: Resultsmentioning

confidence: 99%

Early embryogenesis and organogenesis in the annelidOwenia fusiformis

Carrillo-Baltodano

Seudre

Guynes

et al. 2021

Preprint

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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 °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. 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 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.

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Section: Resultsmentioning

confidence: 99%

Early embryogenesis and organogenesis in the annelidOwenia fusiformis

Carrillo-Baltodano

Seudre

Guynes

et al. 2021

Preprint

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show abstract

“…It is possible that the low degree of neuronal complexity is due to the larva's small body size (~50µm) and their short larval life. None of the clusters analysed showed protonephridial staining and classical protonephridial marker genes (e.g., pou3, sall, lhx1/5) are not expressed in any cluster (17). Protonephridia were also not found in previous studies using immunohistochemistry against acetylated tubulin (15).…”

Section: Oyster Trochophores Have Two Ciliary Bands a Reduced Apical ...mentioning

confidence: 66%

“…Protonephridial markers such as pou2/3, hunchback and six1/2-2 allowed us to identify a cluster of protonephridial cells in the Müller's larva (Fig. 3) (17). Cells from this cluster also express cubulin (specifically expressed in tubule cells of planarian protonephridia), nephrin (nphn-1) and zo2 (34).…”

Section: The Müller's Larva Has Simple Set Of Muscle Types and A Comp...mentioning

confidence: 99%

Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Piovani

Leite

Yáñez-Guerra

et al. 2023

Preprint

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Pelagic larval stages are widespread across animals, yet it is unclear if larvae were present in the last common ancestor of animals or whether they evolved multiple times due to common selective pressures. Many marine larvae are at least superficially similar, they are small, swim through beating of ciliated bands and sense the environment with an apical organ structure. To understand these similarities, we have generated single cell atlases for marine larvae from two animal phyla and have compared their cell types. We found clear similarities among ciliary band cells and neurons of the apical organ in the two larvae pointing to possible homology of these structures suggesting a single origin of larvae within the clade analysed here (Lophotrochozoa). We also find several clade specific innovations in each larva, including distinct myocytes and shell gland cells in the oyster larva. Oyster shell gland cells express many novel genes which have made previous gene age estimates for trochophore larvae too young.

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Early embryogenesis and organogenesis in the annelid Owenia fusiformis

Carrillo-Baltodano

Seudre

Guynes

et al. 2021

EvoDevo

View full text Add to dashboard Cite

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.

show abstract

A single origin of animal excretory organs

Cited by 3 publications

References 55 publications

Early embryogenesis and organogenesis in the annelidOwenia fusiformis

Early embryogenesis and organogenesis in the annelidOwenia fusiformis

Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Early embryogenesis and organogenesis in the annelid Owenia fusiformis

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