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Opposing directions of stage-specific body shape change in a close relative of C. elegans

BACKGROUND: Body size is a fundamental organismal trait. However, as body size and ecological contexts change across developmental time, evolutionary divergence may cause unexpected patterns of body size diversity among developmental stages. This may be particularly evident in polyphenic development...

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Autores principales: Hammerschmith, Eric W., Woodruff, Gavin C., Moser, Kimberly A., Johnson, Erik, Phillips, Patrick C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127021/
https://www.ncbi.nlm.nih.gov/pubmed/37170380
http://dx.doi.org/10.1186/s40850-022-00131-y
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author Hammerschmith, Eric W.
Woodruff, Gavin C.
Moser, Kimberly A.
Johnson, Erik
Phillips, Patrick C.
author_facet Hammerschmith, Eric W.
Woodruff, Gavin C.
Moser, Kimberly A.
Johnson, Erik
Phillips, Patrick C.
author_sort Hammerschmith, Eric W.
collection PubMed
description BACKGROUND: Body size is a fundamental organismal trait. However, as body size and ecological contexts change across developmental time, evolutionary divergence may cause unexpected patterns of body size diversity among developmental stages. This may be particularly evident in polyphenic developmental stages specialized for dispersal. The dauer larva is such a stage in nematodes, and Caenorhabditis species disperse by traveling on invertebrate carriers. Here, we describe the morphology of a stress-resistant, dauer-like larval stage of the nematode Caenorhabditis inopinata, whose adults can grow to be nearly twice as long as its close relative, the model organism C. elegans. RESULTS: We find that a dauer-like, stress-resistant larval stage in two isolates of C. inopinata is on average 13% shorter and 30% wider than the dauer larvae of C. elegans, despite its much longer adult stage. Additionally, many C. inopinata dauer-like larvae were ensheathed, a possible novelty in this lineage reminiscent of the infective juveniles of parasitic nematodes. Variation in dauer-like larva formation frequency among twenty-four wild isolates of C. inopinata was also observed, although frequencies were low across all isolates (< 2%), with many isolates unable to produce dauer-like larvae under conventional laboratory conditions. CONCLUSION: Most Caenorhabditis species thrive on rotting plants and disperse on snails, slugs, or isopods (among others) whereas C. inopinata is ecologically divergent and thrives in fresh Ficus septica figs and disperses on their pollinating wasps. While there is some unknown factor of the fig environment that promotes elongated body size in C. inopinata adults, the small size or unique life history of its fig wasp carrier may be driving the divergent morphology of its stress-resistant larval stages. Further characterization of the behavior, development, and morphology of this stage will refine connections to homologous developmental stages in other species and determine whether ecological divergence across multiple developmental stages can promote unexpected and opposing changes in body size dimensions within a single species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00131-y.
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spelling pubmed-101270212023-04-26 Opposing directions of stage-specific body shape change in a close relative of C. elegans Hammerschmith, Eric W. Woodruff, Gavin C. Moser, Kimberly A. Johnson, Erik Phillips, Patrick C. BMC Zool Research BACKGROUND: Body size is a fundamental organismal trait. However, as body size and ecological contexts change across developmental time, evolutionary divergence may cause unexpected patterns of body size diversity among developmental stages. This may be particularly evident in polyphenic developmental stages specialized for dispersal. The dauer larva is such a stage in nematodes, and Caenorhabditis species disperse by traveling on invertebrate carriers. Here, we describe the morphology of a stress-resistant, dauer-like larval stage of the nematode Caenorhabditis inopinata, whose adults can grow to be nearly twice as long as its close relative, the model organism C. elegans. RESULTS: We find that a dauer-like, stress-resistant larval stage in two isolates of C. inopinata is on average 13% shorter and 30% wider than the dauer larvae of C. elegans, despite its much longer adult stage. Additionally, many C. inopinata dauer-like larvae were ensheathed, a possible novelty in this lineage reminiscent of the infective juveniles of parasitic nematodes. Variation in dauer-like larva formation frequency among twenty-four wild isolates of C. inopinata was also observed, although frequencies were low across all isolates (< 2%), with many isolates unable to produce dauer-like larvae under conventional laboratory conditions. CONCLUSION: Most Caenorhabditis species thrive on rotting plants and disperse on snails, slugs, or isopods (among others) whereas C. inopinata is ecologically divergent and thrives in fresh Ficus septica figs and disperses on their pollinating wasps. While there is some unknown factor of the fig environment that promotes elongated body size in C. inopinata adults, the small size or unique life history of its fig wasp carrier may be driving the divergent morphology of its stress-resistant larval stages. Further characterization of the behavior, development, and morphology of this stage will refine connections to homologous developmental stages in other species and determine whether ecological divergence across multiple developmental stages can promote unexpected and opposing changes in body size dimensions within a single species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00131-y. BioMed Central 2022-07-06 /pmc/articles/PMC10127021/ /pubmed/37170380 http://dx.doi.org/10.1186/s40850-022-00131-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Hammerschmith, Eric W.
Woodruff, Gavin C.
Moser, Kimberly A.
Johnson, Erik
Phillips, Patrick C.
Opposing directions of stage-specific body shape change in a close relative of C. elegans
title Opposing directions of stage-specific body shape change in a close relative of C. elegans
title_full Opposing directions of stage-specific body shape change in a close relative of C. elegans
title_fullStr Opposing directions of stage-specific body shape change in a close relative of C. elegans
title_full_unstemmed Opposing directions of stage-specific body shape change in a close relative of C. elegans
title_short Opposing directions of stage-specific body shape change in a close relative of C. elegans
title_sort opposing directions of stage-specific body shape change in a close relative of c. elegans
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127021/
https://www.ncbi.nlm.nih.gov/pubmed/37170380
http://dx.doi.org/10.1186/s40850-022-00131-y
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