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Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus

Marine heatwave (MHW) events, characterized by periods of anomalous temperatures, are an increasingly prevalent threat to coastal marine ecosystems. Given the seasonal phenology of MHWs, the full extent of their biological consequences may depend on how these thermal stress events align with an orga...

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Autores principales: Leach, Terence S., Hofmann, Gretchen E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10436589/
https://www.ncbi.nlm.nih.gov/pubmed/37601631
http://dx.doi.org/10.3389/fphys.2023.1230590
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author Leach, Terence S.
Hofmann, Gretchen E.
author_facet Leach, Terence S.
Hofmann, Gretchen E.
author_sort Leach, Terence S.
collection PubMed
description Marine heatwave (MHW) events, characterized by periods of anomalous temperatures, are an increasingly prevalent threat to coastal marine ecosystems. Given the seasonal phenology of MHWs, the full extent of their biological consequences may depend on how these thermal stress events align with an organism’s reproductive cycle. In organisms with more complex life cycles (e.g., many marine invertebrate species) the alignment of adult and larval environments may be an important factor determining offspring success, setting the stage for MHW events to influence reproduction and development in situ. Here, the influence of MHW-like temperatures on the early development of the California purple sea urchin, Strongylocentrotus purpuratus, were explored within the context of paternal thermal history. Based on temperature data collected during MHW events seen in Southern California from 2014–2020, adult urchins were acclimated to either MHW or non-MHW temperatures for 28 days before their sperm was used to produce embryos that were subsequently raised under varying thermal conditions. Once offspring reached an early larval stage, the impact of paternal and offspring environments were assessed on two aspects of offspring performance: larval size and thermal tolerance. Exposure to elevated temperatures during early development resulted in larger, more thermally tolerant larvae, with further influences of paternal identity and thermal history, respectively. The alignment of paternal and offspring exposure to MHW temperatures had additional positive benefits on larval thermal tolerance, but this tolerance significantly decreased when their thermal experience mismatched. As the highest recorded temperatures within past MHW events have occurred during the gametogenesis of many kelp forest benthic marine invertebrate species, such as the purple sea urchin, such parental mediated impacts may represent important drivers of future recruitment and population composition for these species.
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spelling pubmed-104365892023-08-19 Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus Leach, Terence S. Hofmann, Gretchen E. Front Physiol Physiology Marine heatwave (MHW) events, characterized by periods of anomalous temperatures, are an increasingly prevalent threat to coastal marine ecosystems. Given the seasonal phenology of MHWs, the full extent of their biological consequences may depend on how these thermal stress events align with an organism’s reproductive cycle. In organisms with more complex life cycles (e.g., many marine invertebrate species) the alignment of adult and larval environments may be an important factor determining offspring success, setting the stage for MHW events to influence reproduction and development in situ. Here, the influence of MHW-like temperatures on the early development of the California purple sea urchin, Strongylocentrotus purpuratus, were explored within the context of paternal thermal history. Based on temperature data collected during MHW events seen in Southern California from 2014–2020, adult urchins were acclimated to either MHW or non-MHW temperatures for 28 days before their sperm was used to produce embryos that were subsequently raised under varying thermal conditions. Once offspring reached an early larval stage, the impact of paternal and offspring environments were assessed on two aspects of offspring performance: larval size and thermal tolerance. Exposure to elevated temperatures during early development resulted in larger, more thermally tolerant larvae, with further influences of paternal identity and thermal history, respectively. The alignment of paternal and offspring exposure to MHW temperatures had additional positive benefits on larval thermal tolerance, but this tolerance significantly decreased when their thermal experience mismatched. As the highest recorded temperatures within past MHW events have occurred during the gametogenesis of many kelp forest benthic marine invertebrate species, such as the purple sea urchin, such parental mediated impacts may represent important drivers of future recruitment and population composition for these species. Frontiers Media S.A. 2023-08-04 /pmc/articles/PMC10436589/ /pubmed/37601631 http://dx.doi.org/10.3389/fphys.2023.1230590 Text en Copyright © 2023 Leach and Hofmann. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Leach, Terence S.
Hofmann, Gretchen E.
Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus
title Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus
title_full Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus
title_fullStr Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus
title_full_unstemmed Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus
title_short Marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, Strongylocentrotus purpuratus
title_sort marine heatwave temperatures enhance larval performance but are meditated by paternal thermal history and inter-individual differences in the purple sea urchin, strongylocentrotus purpuratus
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10436589/
https://www.ncbi.nlm.nih.gov/pubmed/37601631
http://dx.doi.org/10.3389/fphys.2023.1230590
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