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Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)

BACKGROUND: Planaxis sulcatus has been touted as a textbook example of poecilogony, with members of this wide-ranging Indo-Pacific marine gastropod said to produce free-swimming veligers as well as brooded juveniles. A recent paper by Wiggering et al. (BMC Evol Biol 20:76, 2020) assessed a mitochond...

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Autores principales: Fassio, Giulia, Bouchet, Philippe, Oliverio, Marco, Strong, Ellen E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8822645/
https://www.ncbi.nlm.nih.gov/pubmed/35130841
http://dx.doi.org/10.1186/s12862-022-01961-7
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author Fassio, Giulia
Bouchet, Philippe
Oliverio, Marco
Strong, Ellen E.
author_facet Fassio, Giulia
Bouchet, Philippe
Oliverio, Marco
Strong, Ellen E.
author_sort Fassio, Giulia
collection PubMed
description BACKGROUND: Planaxis sulcatus has been touted as a textbook example of poecilogony, with members of this wide-ranging Indo-Pacific marine gastropod said to produce free-swimming veligers as well as brooded juveniles. A recent paper by Wiggering et al. (BMC Evol Biol 20:76, 2020) assessed a mitochondrial gene phylogeny based on partial COI and 16S rRNA sequences for 31 individuals supplemented by observations from the brood pouch of 64 mostly unsequenced individuals. ABGD and bGYMC supported three reciprocally monophyletic clades, with two distributed in the Indo-Pacific, and one restricted to the northern Indian Ocean and Red Sea. Given an apparent lack of correlation between clade membership and morphological differentiation or mode of development, the reported 3.08% maximum K2P model-corrected genetic divergence in COI among all specimens was concluded to represent population structuring. Hence, the hypothesis that phylogenetic structure is evidence of cryptic species was rejected and P. sulcatus was concluded to represent a case of geographic poecilogony. RESULTS: Our goal was to reassess the case for poecilogony in Planaxis sulcatus with a larger molecular dataset and expanded geographic coverage. We sequenced an additional 55 individuals and included published and unpublished sequence data from other sources, including from Wiggering et al. Our dataset comprised 108 individuals (88 COI, 81 16S rRNA) and included nine countries unrepresented in the previous study. The expanded molecular dataset yielded a maximum K2P model-corrected genetic divergence among all sequenced specimens of 12.09%. The value of 3.08% erroneously reported by Wiggering et al. is the prior maximal distance value that yields a single-species partition in ABGD, and not the maximum K2P intraspecific divergence that can be calculated for the dataset. The bGMYC analysis recognized between two and six subdivisions, while the best-scoring ASAP partitions recognized two, four, or five subdivisions, not all of which were robustly supported in Bayesian and maximum likelihood phylogenetic analyses of the concatenated and single gene datasets. These hypotheses yielded maximum intra-clade genetic distances in COI of 2.56–6.19%, which are more consistent with hypothesized species-level thresholds for marine caenogastropods. CONCLUSIONS: Based on our analyses of a more comprehensive dataset, we conclude that the evidence marshalled by Wiggering et al. in support of Planaxis sulcatus comprising a single widespread, highly variable species with geographic poecilogony is unconvincing and requires further investigation in an integrative taxonomic framework. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01961-7.
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spelling pubmed-88226452022-02-08 Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae) Fassio, Giulia Bouchet, Philippe Oliverio, Marco Strong, Ellen E. BMC Ecol Evol Research BACKGROUND: Planaxis sulcatus has been touted as a textbook example of poecilogony, with members of this wide-ranging Indo-Pacific marine gastropod said to produce free-swimming veligers as well as brooded juveniles. A recent paper by Wiggering et al. (BMC Evol Biol 20:76, 2020) assessed a mitochondrial gene phylogeny based on partial COI and 16S rRNA sequences for 31 individuals supplemented by observations from the brood pouch of 64 mostly unsequenced individuals. ABGD and bGYMC supported three reciprocally monophyletic clades, with two distributed in the Indo-Pacific, and one restricted to the northern Indian Ocean and Red Sea. Given an apparent lack of correlation between clade membership and morphological differentiation or mode of development, the reported 3.08% maximum K2P model-corrected genetic divergence in COI among all specimens was concluded to represent population structuring. Hence, the hypothesis that phylogenetic structure is evidence of cryptic species was rejected and P. sulcatus was concluded to represent a case of geographic poecilogony. RESULTS: Our goal was to reassess the case for poecilogony in Planaxis sulcatus with a larger molecular dataset and expanded geographic coverage. We sequenced an additional 55 individuals and included published and unpublished sequence data from other sources, including from Wiggering et al. Our dataset comprised 108 individuals (88 COI, 81 16S rRNA) and included nine countries unrepresented in the previous study. The expanded molecular dataset yielded a maximum K2P model-corrected genetic divergence among all sequenced specimens of 12.09%. The value of 3.08% erroneously reported by Wiggering et al. is the prior maximal distance value that yields a single-species partition in ABGD, and not the maximum K2P intraspecific divergence that can be calculated for the dataset. The bGMYC analysis recognized between two and six subdivisions, while the best-scoring ASAP partitions recognized two, four, or five subdivisions, not all of which were robustly supported in Bayesian and maximum likelihood phylogenetic analyses of the concatenated and single gene datasets. These hypotheses yielded maximum intra-clade genetic distances in COI of 2.56–6.19%, which are more consistent with hypothesized species-level thresholds for marine caenogastropods. CONCLUSIONS: Based on our analyses of a more comprehensive dataset, we conclude that the evidence marshalled by Wiggering et al. in support of Planaxis sulcatus comprising a single widespread, highly variable species with geographic poecilogony is unconvincing and requires further investigation in an integrative taxonomic framework. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-022-01961-7. BioMed Central 2022-02-07 /pmc/articles/PMC8822645/ /pubmed/35130841 http://dx.doi.org/10.1186/s12862-022-01961-7 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
Fassio, Giulia
Bouchet, Philippe
Oliverio, Marco
Strong, Ellen E.
Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)
title Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)
title_full Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)
title_fullStr Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)
title_full_unstemmed Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)
title_short Re-evaluating the case for poecilogony in the gastropod Planaxis sulcatus (Cerithioidea, Planaxidae)
title_sort re-evaluating the case for poecilogony in the gastropod planaxis sulcatus (cerithioidea, planaxidae)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8822645/
https://www.ncbi.nlm.nih.gov/pubmed/35130841
http://dx.doi.org/10.1186/s12862-022-01961-7
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