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Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology
BACKGROUND: The pilidium larva is an idiosyncrasy defining one clade of marine invertebrates, the Pilidiophora (Nemertea, Spiralia). Uniquely, in pilidial development, the juvenile worm forms from a series of isolated rudiments called imaginal discs, then erupts through and devours the larval body d...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5299685/ https://www.ncbi.nlm.nih.gov/pubmed/28194219 http://dx.doi.org/10.1186/s12983-017-0189-x |
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author | Hunt, Marie K. Maslakova, Svetlana A. |
author_facet | Hunt, Marie K. Maslakova, Svetlana A. |
author_sort | Hunt, Marie K. |
collection | PubMed |
description | BACKGROUND: The pilidium larva is an idiosyncrasy defining one clade of marine invertebrates, the Pilidiophora (Nemertea, Spiralia). Uniquely, in pilidial development, the juvenile worm forms from a series of isolated rudiments called imaginal discs, then erupts through and devours the larval body during catastrophic metamorphosis. A typical pilidium is planktotrophic and looks like a hat with earflaps, but pilidial diversity is much broader and includes several types of non-feeding pilidia. One of the most intriguing recently discovered types is the lecithotrophic pilidium nielseni of an undescribed species, Micrura sp. “dark” (Lineidae, Heteronemertea, Pilidiophora). The egg-shaped pilidium nielseni bears two transverse circumferential ciliary bands evoking the prototroch and telotroch of the trochophore larva found in some other spiralian phyla (e.g. annelids), but undergoes catastrophic metamorphosis similar to that of other pilidia. While it is clear that the resemblance to the trochophore is convergent, it is not clear how pilidium nielseni acquired this striking morphological similarity. RESULTS: Here, using light and confocal microscopy, we describe the development of pilidium nielseni from fertilization to metamorphosis, and demonstrate that fundamental aspects of pilidial development are conserved. The juvenile forms via three pairs of imaginal discs and two unpaired rudiments inside a distinct larval epidermis, which is devoured by the juvenile during rapid metamorphosis. Pilidium nielseni even develops transient, reduced lobes and lappets in early stages, re-creating the hat-like appearance of a typical pilidium. Notably, its two transverse ciliary bands can be ontogenetically linked to the primary ciliary band spanning the larval lobes and lappets of the typical planktotrophic pilidium. CONCLUSIONS: Our data shows that the development of pilidium nielseni differs remarkably from that of the trochophore, even though their larval morphology is superficially similar. Pilidium nielseni’s morphological and developmental features are best explained by transition from planktotrophy to lecithotrophy in the context of pilidial development, rather than by retention of or reversal to what is often assumed to be the spiralian ancestral larval type — the trochophore. Development of pilidium nielseni is a compelling example of convergent evolution of a trochophore-like body plan within Spiralia. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-017-0189-x) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-5299685 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-52996852017-02-13 Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology Hunt, Marie K. Maslakova, Svetlana A. Front Zool Research BACKGROUND: The pilidium larva is an idiosyncrasy defining one clade of marine invertebrates, the Pilidiophora (Nemertea, Spiralia). Uniquely, in pilidial development, the juvenile worm forms from a series of isolated rudiments called imaginal discs, then erupts through and devours the larval body during catastrophic metamorphosis. A typical pilidium is planktotrophic and looks like a hat with earflaps, but pilidial diversity is much broader and includes several types of non-feeding pilidia. One of the most intriguing recently discovered types is the lecithotrophic pilidium nielseni of an undescribed species, Micrura sp. “dark” (Lineidae, Heteronemertea, Pilidiophora). The egg-shaped pilidium nielseni bears two transverse circumferential ciliary bands evoking the prototroch and telotroch of the trochophore larva found in some other spiralian phyla (e.g. annelids), but undergoes catastrophic metamorphosis similar to that of other pilidia. While it is clear that the resemblance to the trochophore is convergent, it is not clear how pilidium nielseni acquired this striking morphological similarity. RESULTS: Here, using light and confocal microscopy, we describe the development of pilidium nielseni from fertilization to metamorphosis, and demonstrate that fundamental aspects of pilidial development are conserved. The juvenile forms via three pairs of imaginal discs and two unpaired rudiments inside a distinct larval epidermis, which is devoured by the juvenile during rapid metamorphosis. Pilidium nielseni even develops transient, reduced lobes and lappets in early stages, re-creating the hat-like appearance of a typical pilidium. Notably, its two transverse ciliary bands can be ontogenetically linked to the primary ciliary band spanning the larval lobes and lappets of the typical planktotrophic pilidium. CONCLUSIONS: Our data shows that the development of pilidium nielseni differs remarkably from that of the trochophore, even though their larval morphology is superficially similar. Pilidium nielseni’s morphological and developmental features are best explained by transition from planktotrophy to lecithotrophy in the context of pilidial development, rather than by retention of or reversal to what is often assumed to be the spiralian ancestral larval type — the trochophore. Development of pilidium nielseni is a compelling example of convergent evolution of a trochophore-like body plan within Spiralia. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-017-0189-x) contains supplementary material, which is available to authorized users. BioMed Central 2017-02-08 /pmc/articles/PMC5299685/ /pubmed/28194219 http://dx.doi.org/10.1186/s12983-017-0189-x Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Hunt, Marie K. Maslakova, Svetlana A. Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
title | Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
title_full | Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
title_fullStr | Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
title_full_unstemmed | Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
title_short | Development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
title_sort | development of a lecithotrophic pilidium larva illustrates convergent evolution of trochophore-like morphology |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5299685/ https://www.ncbi.nlm.nih.gov/pubmed/28194219 http://dx.doi.org/10.1186/s12983-017-0189-x |
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