Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Front Physiol
2023 Jan 01;14:1230590. doi: 10.3389/fphys.2023.1230590.
Show Gene links
Show Anatomy links
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 TS
,
Hofmann GE
.
???displayArticle.abstract???
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.
FIGURE 1. Experimental Design. Across three rounds, male purple sea urchins (Strongylocentrotus purpuratus) were acclimated to either a non-MHW (14°C) or MHW-like (20°C) temperature treatment for 28 days. In each round, sperm from individual males (n = 3 male urchins/temperature treatment) were collected and crossed with pooled eggs from five female urchins in a split-clutch breeding design. Fertilizations by each male and the resulting embryos were then raised under the same non-MHW (13°C) and MHW-like (20°C) temperature conditions experienced during adult acclimation. Offspring were raised under these conditions, in duplicate culture vessels, until being sampled at the echinopluteus larval stage for various performance metrics.
FIGURE 2. Effect of paternal acclimation (non-MHW, 14°C; MHW-like, 20°C) and larval rearing temperature (non-MHW, 13°C; MHW-like, 20°C) treatments on the lethal thermal limit (LT50) of echinopluteus larvae in the purple sea urchin, Strongylocentrotus purpuratus. Data points represent average LT50 across larvae from individual males (n = 9 male urchins/paternal treatment) and error bars represent mean ± standard error.
FIGURE 3. Effect of paternal and offspring temperature treatments on larval arm length in the purple sea urchin, Strongylocentrotus purpuratus. Bars show standard error of the mean. Different letters denote significant differences (p < 0.001) in arm length between treatments, based on a post hoc Tukey test.
FIGURE 4. The effect of individual male identity and larval temperature treatment (14°C or 20°C) on echinopluteus arm length in the purple sea urchin, Strongylocentrotus purpuratus. Datapoints represent average arm lengths of offspring produced by individual sires (n = 9 individual male urchins/paternal treatment) and plots are separated by paternal acclimation temperatures, non-MHW (14°C) and MHW-like (20°C). Error bars are representative of mean ± standard error. ANOVA results with significant p-values are displayed on the graph.
Abdelgalil,
Sea urchin sperm exploit extremum seeking control to find the egg.
2022, Pubmed,
Echinobase
Abdelgalil,
Sea urchin sperm exploit extremum seeking control to find the egg.
2022,
Pubmed
,
Echinobase
Allen,
Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages.
2008,
Pubmed
Amaya,
Bottom marine heatwaves along the continental shelves of North America.
2023,
Pubmed
Byrne,
Vulnerability of the calcifying larval stage of the Antarctic sea urchin Sterechinus neumayeri to near-future ocean acidification and warming.
2013,
Pubmed
,
Echinobase
Byrne,
Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios.
2009,
Pubmed
,
Echinobase
Chan,
Effects of ocean-acidification-induced morphological changes on larval swimming and feeding.
2011,
Pubmed
,
Echinobase
Crean,
What is a paternal effect?
2014,
Pubmed
Crean,
Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance.
2013,
Pubmed
de Vries,
Development and application of a species sensitivity distribution for temperature-induced mortality in the aquatic environment.
2008,
Pubmed
Donelson,
Transgenerational plasticity and climate change experiments: Where do we go from here?
2018,
Pubmed
Eirin-Lopez,
Marine Environmental Epigenetics.
2019,
Pubmed
Frölicher,
Marine heatwaves under global warming.
2018,
Pubmed
Hammond,
Thermal tolerance of Strongylocentrotus purpuratus early life history stages: mortality, stress-induced gene expression and biogeographic patterns.
2010,
Pubmed
,
Echinobase
Harvell,
Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides).
2019,
Pubmed
,
Echinobase
Immler,
The sperm factor: paternal impact beyond genes.
2018,
Pubmed
Jiang,
Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos.
2013,
Pubmed
Lane,
Trans-generational responses to low pH depend on parental gender in a calcifying tubeworm.
2015,
Pubmed
Leuchtenberger,
The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization.
2022,
Pubmed
,
Echinobase
Lymbery,
Post-ejaculation thermal stress causes changes to the RNA profile of sperm in an external fertilizer.
2020,
Pubmed
Lymbery,
The thermal environment of sperm affects offspring success: a test of the anticipatory paternal effects hypothesis in the blue mussel.
2021,
Pubmed
Marshall,
Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects.
2015,
Pubmed
Michaud,
The Blob marine heatwave transforms California kelp forest ecosystems.
2022,
Pubmed
Minuti,
Capacity of an ecologically key urchin to recover from extreme events: Physiological impacts of heatwaves and the road to recovery.
2021,
Pubmed
,
Echinobase
Mousseau,
The adaptive significance of maternal effects.
1998,
Pubmed
O'Connor,
Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation.
2007,
Pubmed
Oliver,
Longer and more frequent marine heatwaves over the past century.
2018,
Pubmed
Palombo,
Thanks mum. Maternal effects in response to ocean acidification of sea urchin larvae at different ecologically relevant temperatures.
2023,
Pubmed
,
Echinobase
Parker,
Adult exposure to ocean acidification is maladaptive for larvae of the Sydney rock oyster Saccostrea glomerata in the presence of multiple stressors.
2017,
Pubmed
Pearse,
Ecological role of purple sea urchins.
2006,
Pubmed
,
Echinobase
Przeslawski,
A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae.
2015,
Pubmed
Reed,
Extreme warming challenges sentinel status of kelp forests as indicators of climate change.
2016,
Pubmed
Rogers-Bennett,
Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens.
2019,
Pubmed
,
Echinobase
Rühmkorff,
Marine heatwaves and upwelling shape stress responses in a keystone predator.
2023,
Pubmed
,
Echinobase
Runcie,
Genetics of gene expression responses to temperature stress in a sea urchin gene network.
2012,
Pubmed
,
Echinobase
Sanford,
Widespread shifts in the coastal biota of northern California during the 2014-2016 marine heatwaves.
2019,
Pubmed
Sconzo,
Activation by heat shock of hsp70 gene transcription in sea urchin embryos.
1995,
Pubmed
,
Echinobase
Sen Gupta,
Drivers and impacts of the most extreme marine heatwaves events.
2020,
Pubmed
Seuront,
Decreased thermal tolerance under recurrent heat stress conditions explains summer mass mortality of the blue mussel Mytilus edulis.
2019,
Pubmed
Sheppard Brennand,
Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla.
2010,
Pubmed
,
Echinobase
Shi,
Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius.
2020,
Pubmed
,
Echinobase
Takayama,
Heat-shock proteins as regulators of apoptosis.
2003,
Pubmed
Uller,
Developmental plasticity and the evolution of parental effects.
2008,
Pubmed
Waite,
Negative carry-over effects on larval thermal tolerances across a natural thermal gradient.
2022,
Pubmed
Wernberg,
Climate-driven regime shift of a temperate marine ecosystem.
2016,
Pubmed
Yin,
Transgenerational effects benefit offspring across diverse environments: a meta-analysis in plants and animals.
2019,
Pubmed
Yorke,
Sea urchins mediate the availability of kelp detritus to benthic consumers.
2019,
Pubmed
,
Echinobase