Parental early life environments drive transgenerational plasticity of offspring metabolism in a freshwater fish (<i>Danio rerio</i>)

Massey, Melanie D.; Dalziel, Anne C.

doi:10.1098/rsbl.2023.0266

Cited by 4 publications

(2 citation statements)

References 49 publications

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“…Furthermore, temperature conditions experienced by parents were shown to confer metabolic compensation in their offspring as a transgenerational response in this species (Massey and Dalziel, 2023). Finally, as the olfactory fear response is innate in zebrafish (Jesuthasan and Mathuru, 2008) it can be observed in its simplest form without the need for learning experiences to occur.…”

Section: Introductionmentioning

confidence: 96%

“…The neuronal circuitry governing olfactory-mediated processes has been extensively described in this model species (Friedrich, Jacobson and Zhu, 2010) thanks to the engineering of genetically encoded calcium indicators that allow brain activity to be observed at the larval stage, when the brain has functional yet less complex neuronal networks than the adult stage (Kettunen, 2012). Furthermore, temperature conditions experienced by parents were shown to confer metabolic compensation in their offspring as a transgenerational response in this species (Massey and Dalziel, 2023). Finally, as the olfactory fear response is innate in zebrafish (Jesuthasan and Mathuru, 2008) it can be observed in its simplest form without the need for learning experiences to occur.…”

Section: Introductionmentioning

confidence: 99%

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Parental thermal conditions affect the brain activity response to alarm cue in larval zebrafish

Sourisse,

Semmelhack,

Schunter

2024

Preprint

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With temperature being a crucial factor affecting the physiology of ectothermic animals, global warming will likely impact neural mechanisms aquatic organisms use to perceive their environment over generations. However, exposure to elevated temperature during specific life stages and across generations may confer fish resilience through phenotypic plasticity. In this study, we investigate the effects of developmental and parental temperature on brain activity response to an olfactory cue in the larval zebrafish,Danio rerio. We exposed parents during reproduction and their offspring during development to control (28°C) or elevated temperature (30°C) and observed the response of the larval telencephalon to an alarm cue using live calcium imaging. Parental exposure to elevated temperature decreased the time till maximum brain activity response regardless of the offspring’s developmental temperature, revealing that parental thermal conditions can affect the excitability of the offspring’s neural circuitry. Furthermore, brain activity duration was affected by the interaction between parental and offspring thermal conditions, tending to last longer when either parents or offspring were exposed to elevated temperature, yet more similar to control when elevated temperature was experienced by both parents and offspring. This could represent an anticipatory parental effect influencing the offspring’s brain response to match the parental environment, or an early developmental effect occurring within a susceptible short time window post-fertilization. Overall, our results suggest that future predicted warming can alter processes involved in brain transmission and show that parental conditions could aid in the preparation of their offspring to respond to olfactory stimuli in a changing environment.

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Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Parental thermal conditions affect the brain activity response to alarm cue in larval zebrafish

Sourisse,

Semmelhack,

Schunter

2024

Preprint

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Parental early life environments drive transgenerational plasticity of offspring metabolism in a freshwater fish (Danio rerio)

Massey,

Dalziel

2023

Biol. Lett.

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Parental experiences can lead to changes in offspring phenotypes through transgenerational plasticity (TGP). TGP is expected to play a role in improving the responses of offspring to changes in climate, but little is known about how the early lives of parents influence offspring TGP. Here, we use a model organism, zebrafish ( Danio rerio ), to contrast the effects of early and later life parental thermal environments on offspring routine metabolism. To accomplish this, we exposed both parents to either constant optimal (27°C) or environmentally realistic diel fluctuating (22–32°C) temperatures during early (embryonic and larval) and later (juvenile and adult) life in a factorial design. We found significant reduction of routine metabolic rates (greater than 20%) at stressful temperatures (22°C and 32°C) after biparental early life exposure to fluctuating temperatures, but little effect of later life parental temperatures on offspring metabolism. This reduction reflects metabolic compensation and is expected to enhance offspring body sizes under stressful temperatures. These changes occur over and above the effects of parental environments on egg size, suggesting alternate non-genetic mechanisms influenced offspring metabolic rates.

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Developmental programming of sarcoplasmic reticulum function improves cardiac anoxia tolerance in turtles

Ruhr,

Shiels,

Crossley

et al. 2024

Journal of Experimental Biology

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Oxygen deprivation during embryonic development can permanently remodel the vertebrate heart, often causing cardiovascular abnormalities in adulthood. While this phenomenon is mostly damaging, recent evidence suggests developmental hypoxia produces stress-tolerant phenotypes in some ectothermic vertebrates. Embryonic common snapping turtles (Chelydra serpentina) subjected to chronic hypoxia display improved cardiac anoxia tolerance after hatching, which is associated with altered Ca2+ homeostasis in heart cells (cardiomyocytes). Here, we examined the possibility that changes in Ca2+ cycling, through the sarcoplasmic reticulum (SR), underlie the developmentally programmed cardiac phenotype of snapping turtles. We investigated this hypothesis by isolating cardiomyocytes from juvenile turtles that developed in either normoxia (21% O2; ‘N21’) or chronic hypoxia (10% O2; ‘H10’) and subjected the cells to anoxia/reoxygenation, in either the presence or absence of SR Ca2+-cycling inhibitors. We simultaneously measured cellular shortening, intracellular Ca2+ concentration ([Ca2+]i), and intracellular pH (pHi). Under normoxic conditions, N21 and H10 cardiomyocytes shortened equally, but H10 Ca2+ transients (Δ[Ca2+]i) were twofold smaller than those of N21 cells, and SR inhibition only decreased N21 shortening and Δ[Ca2+]i. Anoxia subsequently depressed shortening, Δ[Ca2+]i and pHi in control N21 and H10 cardiomyocytes, yet H10 shortening and Δ[Ca2+]i recovered to pre-anoxic levels, partly due to enhanced myofilament Ca2+ sensitivity. SR blockade abolished the recovery of anoxic H10 cardiomyocytes and potentiated decreases in shortening, Δ[Ca2+]i and pHi. Our novel results provide the first evidence of developmental programming of SR function and demonstrate that developmental hypoxia confers a long-lasting, superior anoxia-tolerant cardiac phenotype in snapping turtles, by modifying SR function and enhancing myofilament Ca2+ sensitivity.

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Parental early life environments drive transgenerational plasticity of offspring metabolism in a freshwater fish (Danio rerio)

Cited by 4 publications

References 49 publications

Parental thermal conditions affect the brain activity response to alarm cue in larval zebrafish

Parental thermal conditions affect the brain activity response to alarm cue in larval zebrafish

Parental early life environments drive transgenerational plasticity of offspring metabolism in a freshwater fish (Danio rerio)

Developmental programming of sarcoplasmic reticulum function improves cardiac anoxia tolerance in turtles

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