The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution

Degnan, Sandie M.; Degnan, Bernard M.

doi:10.1098/rstb.2009.0248

Cited by 71Marine Invertebrate Physiology and EcologyMarine Sponges and Natural ProductsDevelopmental Biology and Gene Regulation

The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution

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Degnan, Sandie M., Degnan, Bernard M.·2010·Philosophical Transactions of the Royal Society B: Biological Sciences

DOI 10.1098/rstb.2009.0248PMC PMC2817140

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Abstract

Comparative genomics of representative basal metazoans leaves little doubt that the most recent common ancestor to all modern metazoans was morphogenetically complex. Here, we support this interpretation by demonstrating that the demosponge Amphimedon queenslandica has a biphasic pelagobenthic life cycle resembling that present in a wide range of bilaterians and anthozoan cnidarians. The A. queenslandica life cycle includes a compulsory planktonic larval phase that can end only once the larva develops competence to respond to benthic signals that induce settlement and metamorphosis. The temporal onset of competence varies between individuals as revealed by idiosyncratic responses to inductive cues. Thus, the biphasic life cycle with a dispersing larval phase of variable length appears to be a metazoan synapomorphy and may be viewed as an ancestral polyphenic trait. Larvae of a particular age that are subjected to an inductive cue either maintain the larval form or metamorphose into the post-larval/juvenile form. Variance in the development of competence dictates that only a subset of a larval cohort will settle and undergo metamorphosis at a given time, which in turn leads to variation in dispersal distance and in location of settlement. Population divergence and allopatric speciation are likely outcomes of this conserved developmental polyphenic trait.

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Neuroendocrine signalling during larval settlement and metamorphosis employs the same or homologous molecules, including nitric oxide and Wamide neuropeptides, suggesting deep evolutionary conservation.
“The neuroendocrine signalling during larval settlement and metamorphosis employs the same or homologous signalling molecules, including nitric oxide (NO) and Wamide neuropeptides [77,79,80], suggesting deep evolutionary conservation [81].”
From An option space for early neural evolution (2015) · cites this paper as [79]

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Authors: Degnan, S. M., & Degnan, B. M.
Affiliations: School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia
Venue: Philosophical Transactions of the Royal Society B: Biological Sciences
Publisher: The Royal Society
Published: 2010-02-27
Volume: 365
Issue: 1540
Pages: 641-651
ISSN: 0962-8436 (ISSN-L)
1471-2970
DOI: 10.1098/rstb.2009.0248
PMC: PMC2817140
OpenAlex: W2119848352
Cited by: 71
References: 101
Citations by year: 2026: 6 · 2025: 6 · 2024: 5 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 12 · 2019: 2 · 2018: 4 · 2017: 1 · 2016: 8 · 2015: 4 · 2013: 2 · 2012: 6
FWCI: 0.60
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations: Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: metamorphosis, polyphenism, Amphimedon queenslandica, demosponges, biphasic life cycle, planktotrophy, larval competence, settlement induction, animal evolution, ancestral traits, dispersal distance, allopatric speciation, comparative genomics
MeSH terms: Animals, Biological Evolution, Larva, Life Cycle Stages, Metamorphosis, Biological, Models, Biological, Phenotype, Porifera, Gastrulation

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The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution

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