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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This content will become publicly available on July 21, 2024
Transgenerational plasticity as a mechanism of response to marine heatwaves in the purple sea urchin, Strongylocentrotus purpuratus
Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin ( Strongylocentrotus purpuratus ) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT 50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting.
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- Award ID(s):
- 2131283
- NSF-PAR ID:
- 10445686
- Date Published:
- Journal Name:
- Frontiers in Marine Science
- Volume:
- 10
- ISSN:
- 2296-7745
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Marine heatwaves (MHWs) are projected to increase in intensity and frequency over the coming decades, and it is imperative to assess the adaptive capacity of marine organisms to these extreme temperature events. Given the nature of MHWs to last days to weeks in a region, these events may have overarching impacts on phenological events like reproduction and development. Here, the role of adult thermal history and transgenerational plasticity may be an important pathway by which MHWs are transduced to impact community structure. In this study, we sought to explore the effects of paternal thermal history in the purple urchin,
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A free
Plain Language Summary can be found within the Supporting Information of this article.
