Transgenerational effects of ocean warming on the sea urchin Strongylocentrotus intermedius

Zhao, Chong; Zhang, Lisheng; Shi, Dongtao; Ding, Jingyun; Yin, Donghong; Sun, Jiangnan; Zhang, Baojing; Zhang, Lingling; Chang, Yaqing

doi:10.1016/j.ecoenv.2018.01.014

Cited by 40 publications

(42 citation statements)

References 25 publications

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“…Long-term thermal experience of parents has significant impacts on the embryo development of sea urchins 7,15,18 . Our previous study, for example, showed that the embryo development was significantly influenced at ~27 hours after fertilization in S. intermedius, whose parents were exposed to long-term elevated temperature 15 . The molecular basis, however, remains mostly unknown.…”

Section: Discussionmentioning

confidence: 99%

“…The development of their embryo is significantly affected by high temperatures, greatly affecting their continuation 11,14 . Our previous study found negative transgenerational effects in hatchability and most traits of larval size of the sea urchin Strongylocentrotus intermedius whose parents were exposed to a + ~3 °C temperature for ~15 months 15 . This clearly indicates the TE of ocean warming on embryo development and larval size of S. intermedius.…”

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confidence: 99%

“…In addition, the abundant genetic information of embryo development can greatly support analyses after the sequencing in the present investigation, because sea urchin is a well-known research model of developmental biology. For example, hepatocyte nuclear factor (hnf6) 16 and heat shock protein (hsp70) 17 have been well documented in sea urchin development 15,18,19 . The main purposes of the present study are to investigate 1) how TE of high temperature affects gene expressions of embryos of S. intermedius (transgenerational effect) and 2) how the developmental temperature influences gene expressions of embryos of S. intermedius (developmental temperature effect).…”

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Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius

Shi

Zhao

Chen

et al. 2020

Sci Rep

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Ocean warming increasingly endangers the fitness of marine invertebrates. Transgenerational effects (TE) potentially mitigate the impacts of environmental stress on the embryos of marine invertebrates. The molecular mechanisms, however, remain largely unknown. Using high-throughput RNA sequencing technology, we investigated the gene expression patterns of embryos (the gastrula stage) of the sea urchin Strongylocentrotus intermedius at different developmental temperatures, whose parents were exposed to long-term (15 months) elevated temperature (A) or not (B). The temperatures at which adults were held for ~4 weeks prior to the start of the experiment (21 °C for A and 18 °C for B) were also used for the development of offspring (high: 21 °C and ambient (laboratory): 18 °C) resulting in four experimental groups (HA and HB at 21 °C, and LA and LB at 18 °C). The embryos were sampled ~24 h after fertilization. All samples were in the gastrula stage. Twelve mRNA libraries (groups HA, HB, LA, LB, 3 replicates for each group) were established for the following sequencing. Embryos whose parents were exposed to elevated temperatures or not showed 1891 significantly different DEGs (differentially expressed genes) at the ambient developmental temperature (LB vs LA, LB as control) and 2203 significantly different DEGs at the high developmental temperature (HB vs HA, HB as control), respectively. This result indicates complex molecular mechanisms of transgenerational effects of ocean warming, in which a large number of genes are involved. With the TE, we found 904 shared DEGs in both LB vs LA (LB as control) and HB vs HA (HB as control) changed in the same direction of expression (i.e., up-or down-regulated), indicating that parental exposed temperatures affect the expression of these genes in the same manner regardless of the development temperature. With developmental exposure, we found 198 shared DEGs in both HB vs LB (HB as control) and HA vs LA (HA as control) changed in the same direction of expression. Of the 198 DEGs, more genes were up-regulated at high developmental temperature. Interestingly, embryos whose parents were exposed to high temperature showed fewer differently expressed DEGs between high and low developmental temperatures than the individuals whose parents were exposed to ambient temperature. The results indicate that gene expressions are probably depressed by the transgenerational effect of ocean warming. The roles of hsp70 and hnf6 in thermal acclimation are highlighted for future studies. The present study provides new insights into the molecular mechanisms of the transgenerational and developmental effects of ocean warming on the embryos of sea urchins. Ocean warming is an increasing threat to the fitness of marine invertebrates because the water temperature is predicted to rise 2-4 °C over the next century by the Intergovernmental Panel on Climate Change (IPCC) 1. Marine

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Section: Discussionmentioning

confidence: 99%

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Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius

Shi

Zhao

Chen

et al. 2020

Sci Rep

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“…As shown for S. glomerata , production of commercial bivalves that are more resilient to global change stressors, in tandem with advances from selective breeding efforts, hold promise in designing strategies for evolutionary rescue of key aquaculture resources to help climate proof shellfish industries. A better understanding of calcification physiology and mechanisms is needed, as recent studies show that this process is phenotypically plastic and can be adjusted with respect to environmental conditions (Fitzer et al, , , ; Zhao, Zhang, et al, ).…”

Section: Insights From Aquaculture Practice Via Epigenetic Selectionmentioning

confidence: 99%

Limitations of cross‐ and multigenerational plasticity for marine invertebrates faced with global climate change

Byrne

Foo

Ross

et al. 2019

Global Change Biology

121

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Although cross generation (CGP) and multigenerational (MGP) plasticity have been identified as mechanisms of acclimation to global change, the weight of evidence indicates that parental conditioning over generations is not a panacea to rescue stress sensitivity in offspring. For many species, there were no benefits of parental conditioning. Even when improved performance was observed, this waned over time within a generation or across generations and fitness declined. CGP and MGP studies identified resilient species with stress tolerant genotypes in wild populations and selected family lines. Several bivalves possess favourable stress tolerance and phenotypically plastic traits potentially associated with genetic adaptation to life in habitats where they routinely experience temperature and/or acidification stress. These traits will be important to help 'climate proof' shellfish ventures. Species that are naturally stress tolerant and those that naturally experience a broad range of environmental conditions are good candidates to provide insights into the physiological and molecular mechanisms involved in CGP and MGP. It is challenging to conduct ecologically relevant global change experiments over the long times commensurate with the pace of changing climate. As a result, many studies present stressors in a shock-type exposure at rates much faster than projected scenarios. With more gradual stressor introduction over longer experimental durations and in context with conditions species are currently acclimatized and/or adapted to, the outcomes for sensitive species might differ. We highlight the importance to understand primordial germ cell development and the timing of gametogenesis with respect to stressor exposure. Although multigenerational exposure to global change stressors currently appears limited as a universal tool to rescue species in the face of changing climate, natural proxies of future conditions (upwelling zones, CO 2 vents, naturally warm habitats) show that phenotypic adjustment and/or beneficial genetic selection is possible for some species, indicating complex plasticity-adaptation interactions. K E Y W O R D Sadaptation, habitat warming, ocean acidification, phenotypic plasticity, stress resilience | 81 BYRNE Et al.

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“…The capability of adult individuals to acclimatize and endure thermal changes is highly relevant from an evolutionary perspective. It not only affects their own physiological performance and/or the quality of their gametes, but it can also result in negative transgenerational carry-over effects on hatchability and larval size of the next generation, which have been shown after prolonged periods of parental exposure to elevated temperatures in some sea urchins (Zhao et al, 2018). In sea urchins, transcriptomes from different tissue types and larval thermal stress responses have been characterized (e.g., Clark et al, 2019;Gaitán-Espitia, Sánchez, Bruning, & Cárdenas, 2016;Gillard, Garama, & Brown, 2014;Jia et al, 2017;Pérez-Portela, Turon, & Riesgo, 2016;Runcie et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Enjoying the warming Mediterranean: Transcriptomic responses to temperature changes of a thermophilous keystone species in benthic communities

et al. 2020

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Information about the genomic processes underlying responses to temperature changes is still limited in non‐model marine invertebrates. In this sense, transcriptomic analyses can help to identify genes potentially related to thermal responses. We here investigated, via RNA‐seq, whole‐transcriptomic responses to increased and decreased temperatures in a thermophilous keystone sea urchin, Arbacia lixula, whose populations are increasing in the Mediterranean. This species is a key driver of benthic communities’ structure due to its grazing activity. We found a strong response to experimentally induced cold temperature (7°C), with 1,181 differentially expressed transcripts relative to the control condition (13°C), compared to only 179 in the warm (22°C) treatment. A total of 84 (cold treatment) and three (warm treatment) gene ontology terms were linked to the differentially expressed transcripts. At 7°C the expression of genes encoding different heat shock proteins (HSPs) was upregulated, together with apoptotic suppressor genes (e.g., Bcl2), genes involved in the infection response and/or pathogen‐recognition (e.g., echinoidin) and ATP‐associated genes, while protein biosynthesis and DNA replication pathways were downregulated. At 22°C neither HSPs induction nor activation of the previously mentioned pathways were detected, with the exception of some apoptotic‐related activities that were upregulated. Our results suggest a strong transcriptional response associated with low temperatures, and support the idea of low water temperature being a major limitation for A. lixula expansion across deep Mediterranean and northern Atlantic waters.

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Transgenerational effects of ocean warming on the sea urchin Strongylocentrotus intermedius

Cited by 40 publications

References 25 publications

Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius

Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius

Limitations of cross‐ and multigenerational plasticity for marine invertebrates faced with global climate change

Enjoying the warming Mediterranean: Transcriptomic responses to temperature changes of a thermophilous keystone species in benthic communities

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