Divergent Carry-Over Effects of Hypoxia during the Early Development of Abalone.

After being exposed to environmental stimuli during early developmental stages, some organisms may gain or weaken physiological regulating abilities, which would have long-lasting effects on their performance. Environmental hypoxia events can have significant effects on marine organisms, but for breeding programs and other practical applications, it is important to further explore the long-term physiological effects of early hypoxia exposure in economically significant species. In this study, the Pacific abalone Haliotis discus hannai was exposed to moderate hypoxia (∼4 mg/L) from zygote to trochophora, and the assessments of hypoxia tolerance were conducted on the grow-out stage. The results revealed that juvenile abalones exposed to hypoxia at the early development stages were more hypoxia-tolerant but with slower weight growth, a phenomenon called the trade-off between growth and survival. These phenotypic effects driven by the hypoxia exposure were explained by strong selection of genes involved in signal transduction, autophagy, apoptosis, and hormone regulation. Moreover, long non-coding RNA regulation plays an important role modulating carry-over effects by controlling DNA replication and repair, signal transduction, myocardial activity, and hormone regulation. This study revealed that the ability to create favorable phenotypic differentiation through genetic selection and/or epigenetic regulation is important for the survival and development of aquatic animals in the face of rapidly changing environmental conditions.

• Publication year

  2022

• Venue

  Environmental Science and Technology

• Publication date

  2022-12-08

• Fields of study

  Medicine, Environmental Science

• Identifiers
  DOI 10.1021/acs.est.2c04975PMID 36479946
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Long-read RNA sequencing of Pacific abalone Haliotis discus hannai reveals innate immune system responses to environmental stress.

  2022cited by this paper
• Transcriptome profiling of the early developmental stages in the giant mussel Choromytilus chorus exposed to delousing drugs.

  2022cited by this paper
• Genome-Wide Identification of Long Non-coding RNAs in Crassostrea gigas and Their Association with Heat Stress

  2022cited by this paper
• Comparative Transcriptome Analysis of Heart Tissue in Response to Hypoxia in Silver Sillago (Sillago sihama)

  2021cited by this paper
• Benchmarking the performance of Pool‐seq SNP callers using simulated and real sequencing data

  2021cited by this paper
• Aquatic foods to nourish nations

  2021cited by this paper
• Analysis of lncRNA and mRNA expression profiles in peripheral blood leukocytes of the half-smooth tongue sole (Cynoglossus semilaevis) treated with chitosan oligosaccharide.

  2021cited by this paper
• Distinct metabolic shifts occur during the transition between normoxia and hypoxia in the hybrid and its maternal abalone.

  2021cited by this paper
• Oxidative stress induced by methomyl exposure reduces the quality of early embryo development in mice.

  2021cited by this paper
• Integrated Analysis of Coding Genes and Non-coding RNAs Associated with Shell Color in the Pacific Oyster (Crassostrea gigas)

  2021cited by this paper
• Context‐dependent carryover effects of hypoxia and warming in a coastal ecosystem engineer

  2021cited by this paper
• Differential Expression of Long Non-Coding RNA (lncRNA) in Mediterranean Mussel (Mytilus galloprovincialis) Hemocytes under Immune Stimuli

  2021cited by this paper
• A new indicator of hypoxia tolerance in abalone, developed based on heart rate fluctuations

  2020cited by this paper
• Stress across life stages: Impacts, responses and consequences for marine organisms.

  2020cited by this paper
• The effects of constant and cyclical hypoxia on the survival, growth and metabolic physiology of incubating Atlantic salmon (Salmo salar)

  2020cited by this paper
• Both maternal and embryonic exposure to mild hypoxia influence embryonic development of the intertidal gastropod Littorina littorea

  2020cited by this paper
• Evolved differences in energy metabolism and growth dictate the impacts of ocean acidification on abalone aquaculture

  2020cited by this paper
• Prolonged exposure to hypoxia inhibits the growth of Pacific abalone by modulating innate immunity and oxidative status.

  2020cited by this paper
• A beginner's guide to low‐coverage whole genome sequencing for population genomics

  2020cited by this paper
• ggalluvial: Layered Grammar for Alluvial Plots

  2020cited by this paper
• Immunity-associated long non-coding RNA and expression in response to bacterial infection in large yellow croaker (Larimichthys crocea).

  2019cited by this paper
• Limitations of cross‐ and multigenerational plasticity for marine invertebrates faced with global climate change

  2019cited by this paper
• Recommendations for performance optimizations when using GATK3.8 and GATK4

  2019cited by this paper
• Regulation of gene expression by cis-acting long non-coding RNAs

  2019cited by this paper
• Hypoxia Causes Transgenerational Impairment of Ovarian Development and Hatching Success in Fish.

  2019cited by this paper
• Combined effects of warming and hypoxia on early life stage Chinook salmon physiology and development

  2019cited by this paper
• Comparing Pool‐seq, Rapture, and GBS genotyping for inferring weak population structure: The American lobster (Homarus americanus) as a case study

  2019cited by this paper
• Divergence and plasticity shape adaptive potential of the Pacific oyster

  2018cited by this paper
• PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files

  2018cited by this paper
• fastp: an ultra-fast all-in-one FASTQ preprocessor

  2018cited by this paper
• Declining oxygen in the global ocean and coastal waters

  2018cited by this paper
• Metabolic response to hypoxia in European sea bass (Dicentrarchus labrax) displays developmental plasticity.

  2018cited by this paper
• Short- and long-term effects on growth and expression patterns in response to incubation temperatures in Senegalese sole

  2018cited by this paper
• Moderate hypoxia but not warming conditions at larval stage induces adverse carry-over effects on hypoxia tolerance of European sea bass (Dicentrarchus labrax) juveniles.

  2018cited by this paper
• Measuring Genetic Differentiation from Pool-seq Data

  2018cited by this paper
• Temperature induced variation in gene expression of thyroid hormone receptors and deiodinases of European eel (Anguilla anguilla) larvae.

  2017cited by this paper
• Epigenetics in fish gametes and early embryo

  2017cited by this paper
• Cyclical short-term starvation and refeeding provokes compensatory growth in sub-yearling Siberian sturgeon, Acipenser baerii Brandt, 1869

  2017cited by this paper
• Epigenetic regulation and chromatin remodeling in learning and memory

  2017cited by this paper
• Exposure to an acute hypoxic stimulus during early life affects the expression of glucose metabolism-related genes at first-feeding in trout

  2017cited by this paper
• Citrinin exposure affects oocyte maturation and embryo development by inducing oxidative stress-mediated apoptosis

  2017cited by this paper
• Transcriptomic analysis of maternally provisioned cues for phenotypic plasticity in the annual killifish, Austrofundulus limnaeus

  2017cited by this paper
• Adaptive genomic divergence under high gene flow between freshwater and brackish‐water ecotypes of prickly sculpin (Cottus asper) revealed by Pool‐Seq

  2017cited by this paper
• Identification of long non-coding RNAs in two anthozoan species and their possible implications for coral bleaching

  2017cited by this paper
• Hatchery Conditions do not Negatively Impact Respiratory Response of Early Life-Stage Development in Australian Hybrid Abalone

  2016cited by this paper
• Hypoxia causes transgenerational impairments in reproduction of fish

  2016cited by this paper
• Acute and sub‐lethal exposure to copper oxide nanoparticles causes oxidative stress and teratogenicity in zebrafish embryos

  2016cited by this paper
• Unique features of long non-coding RNA biogenesis and function

  2015cited by this paper
• Assessment of oxidative damage to DNA, transcriptional expression of key genes, lipid peroxidation and histopathological changes in carp Cyprinus carpio L. following exposure to chronic hypoxic and subsequent recovery in normoxic conditions.

  2015cited by this paper
• HISAT: a fast spliced aligner with low memory requirements

  2015cited by this paper
• Emerging roles of long non-coding RNA in root developmental plasticity and regulation of phosphate homeostasis

  2015cited by this paper
• Three-Year Breeding Cycle of Rainbow Trout (Oncorhynchus mykiss) Fed a Plant-Based Diet, Totally Free of Marine Resources: Consequences for Reproduction, Fatty Acid Composition and Progeny Survival

  2015cited by this paper
• Growth and survival in a changing environment: Combined effects of moderate hypoxia and low pH on juvenile bivalve Macoma balthica

  2015cited by this paper
• The effect of temperature on the embryonic development of barramundi, the Australian strain of Lates calcarifer (Bloch) using current hatchery practices

  2015cited by this paper
• StringTie enables improved reconstruction of a transcriptome from RNA-seq reads

  2015cited by this paper
• Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve?

  2015cited by this paper
• Developmental Critical Windows and Sensitive Periods as Three-Dimensional Constructs in Time and Space

  2015cited by this paper
• Hypoxia turns genotypic female medaka fish into phenotypic males

  2014cited by this paper
• The biology of developmental plasticity and the Predictive Adaptive Response hypothesis

  2014cited by this paper
• Can environmental conditions experienced in early life influence future generations?

  2014cited by this paper
• Biological carryover effects: linking common concepts and mechanisms in ecology and evolution

  2014cited by this paper
• Hypoxia-inducible factor-1 mediates adaptive developmental plasticity of hypoxia tolerance in zebrafish, Danio rerio

  2014cited by this paper
• A Comprehensive View of the Epigenetic Landscape. Part II: Histone Post-translational Modification, Nucleosome Level, and Chromatin Regulation by ncRNAs

  2014cited by this paper
• Latent effects of hypoxia on the gastropod Crepidula onyx

  2013cited by this paper
• Fantastically plastic: fish larvae equipped for a new world

  2013cited by this paper
• Incubation temperature induces changes in muscle cellularity and gene expression in Senegalese sole (Solea senegalensis).

  2013cited by this paper
• Variation in rates of early development in Haliotis asinina generate competent larvae of different ages

  2012cited by this paper
• Epigenetic Regulation by Long Noncoding RNAs

  2012cited by this paper
• The genetic differentiation at quantitative trait loci under local adaptation

  2012cited by this paper
• clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters

  2012cited by this paper
• Genome regulation by long noncoding RNAs.

  2012cited by this paper
• Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish

  2012cited by this paper
• Oxidative stress in zebrafish embryos induced by short‐term exposure to bisphenol A, nonylphenol, and their mixture

  2011cited by this paper
• Integrating diverse genomic data using gene sets

  2011cited by this paper
• Carry-over effects as drivers of fitness differences in animals.

  2011cited by this paper
• Responses of threespine stickleback (Gasterosteus aculeatus, L) transcriptome to hypoxia.

  2011cited by this paper
• Developmental trajectories, critical windows and phenotypic alteration during cardio-respiratory development.

  2011cited by this paper
• Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish

  2011cited by this paper
• Sequence analysis Advance Access publication June 7, 2011 The variant call format and VCFtools

  2010cited by this paper
• ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data

  2010cited by this paper
• A global view of genomic information--moving beyond the gene and the master regulator.

  2010cited by this paper
• edgeR: a Bioconductor package for differential expression analysis of digital gene expression data

  2009cited by this paper
• Effects of ocean acidification on the early life history of a tropical marine fish

  2009cited by this paper
• The Sequence Alignment/Map format and SAMtools

  2009cited by this paper
• Early growth conditions, phenotypic development and environmental change

  2008cited by this paper
• Defending against hypoxia: Behavioural, physiological and biochemical strategies of hypoxia survival in nearshore marine sculpins

  2008cited by this paper
• Spreading Dead Zones and Consequences for Marine Ecosystems

  2008cited by this paper
• When density dependence is not instantaneous: theoretical developments and management implications.

  2007cited by this paper
• The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae).

  2007cited by this paper
• Early feeding of carnivorous rainbow trout (Oncorhynchus mykiss) with a hyperglucidic diet during a short period: effect on dietary glucose utilization in juveniles.

  2007cited by this paper
• Widespread endocrine disruption and reproductive impairment in an estuarine fish population exposed to seasonal hypoxia

  2007cited by this paper
• PLINK: a tool set for whole-genome association and population-based linkage analyses.

  2007cited by this paper
• Long term hypoxia suppresses reproductive capacity in the estuarine fish, Fundulus grandis.

  2007cited by this paper
• Larval experience and latent effects--metamorphosis is not a new beginning.

  2006cited by this paper
• Effects of various algal diets and starvation on larval growth and survival of Meretrix meretrix

  2006cited by this paper
• Compensatory growth response of Sparus aurata following different starvation and refeeding protocols

  2006cited by this paper
• Developmental Plasticity in the Thermal Tolerance of Zebrafish Danio rerio

  2006cited by this paper
• The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae)

  2006cited by this paper
• Theoretical and practical advances in genome halving

  2004cited by this paper
• Tradeoffs and the evolution of thermal reaction norms

  2003cited by this paper

• From stress to response: a systematic review of epigenetic pathways underlying gene expression and phenotypic plasticity in aquatic invertebrates

  2026cites this paper
• Physiological responses of abalone (Haliotis spp.) to abiotic stress and diseases: a review

  2025cites this paper
• EPO Enhances Adaptation to Hypoxic Environment in the Freshwater Teleost (Micropterus salmoides) through the PI3K/AKT Pathway.

  2025cites this paper
• Metabolism and hypoxia tolerance of the endangered white abalone (Haliotis sorenseni): Implications for conservation and restoration efforts

  2025cites this paper
• Carryover effects of embryonic hypoxia exposure on adult fitness of the Pacific abalone.

  2024cites this paper
• Carryover effects and feeding behavior of Atlantic surfclams in response to climate change

  2024cites this paper
• A high throughput method to assess the hypoxia tolerance of abalone based on adhesion duration

  2024cites this paper
• Transcriptomic analysis revealed the dynamic response mechanism to acute ammonia exposure in the ivory shell, Babylonia areolata.

  2023cites this paper
• Relative importance of phenotypic plasticity and carryover effects in response to small salinity shifts during oyster aquaculture production

  2023cites this paper