Stickleback embryos use ATP-binding cassette transporters as a buffer against exposure to maternally derived cortisol

Paitz, Ryan T.; Bukhari, Syed; Bell, Alison M.

doi:10.1098/rspb.2015.2838

Cited by 25 publications

(25 citation statements)

References 64 publications

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“…Additionally, developmental effects can occur without direct exposure of offspring to maternal glucocorticoids 38,39 . For example, stickleback embryos are able to buffer themselves from exogenous manipulations of cortisol by actively transporting cortisol out of the egg via ATP-binding cassette transporters 69,71 . This suggests that the effects of maternal predator exposure on offspring behavior [72][73][74] , physiology 75 and embryonic gene transcription 76 in threespine stickleback are not mediated solely by embryonic exposure to maternal cortisol.…”

Section: Discussionmentioning

confidence: 99%

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

McGhee

Paitz

Baker

et al. 2020

Sci Rep

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Predation often has consistent effects on prey behavior and morphology, but whether the physiological mechanisms underlying these effects show similarly consistent patterns across different populations remains an open question. In vertebrates, predation risk activates the hypothalamic-pituitaryadrenal (HPA) axis, and there is growing evidence that activation of the maternal HPA axis can have intergenerational consequences via, for example, maternally-derived steroids in eggs. Here, we investigated how predation risk affects a suite of maternally-derived steroids in threespine stickleback eggs across nine Alaskan lakes that vary in whether predatory trout are absent, native, or have been stocked within the last 25 years. Using liquid chromatography coupled with mass spectroscopy (LC-MS/ MS), we detected 20 steroids within unfertilized eggs. Factor analysis suggests that steroids covary within and across steroid classes (i.e. glucocorticoids, progestogens, sex steroids), emphasizing the modularity and interconnectedness of the endocrine response. Surprisingly, egg steroid profiles were not significantly associated with predator regime, although they were more variable when predators were absent compared to when predators were present, with either native or stocked trout. Despite being the most abundant steroid, cortisol was not consistently associated with predation regime. Thus, while predators can affect steroids in adults, including mothers, the link between maternal stress and embryonic development is more complex than a simple one-to-one relationship between the population-level predation risk experienced by mothers and the steroids mothers transfer to their eggs. Predation is a potent force that shapes phenotypes over evolutionary and developmental time 1,2. A major question in evolutionary biology is the extent to which selective pressures such as predation pressure have predictable effects on prey phenotypes and the role of natural selection in shaping consistent patterns of plasticity and/or the independent evolution of similar traits in closely related lineages (i.e. parallelism 3-6). Examining whether different populations of prey respond to predators in the same manner has offered insights into this question 7. For example, traits that protect prey and/or enable quick escape from predators often show evidence of parallelism across replicate populations with similar predation regimes (e.g. morphology 7,8 ; antipredator behavior 9,10). Predation pressure has also been shown to affect life history traits (e.g. age and size at maturity, offspring size and number), often in a parallel manner across populations with similar predation regimes 11,12. Despite the many studies comparing morphology, behavior, and life history traits among populations that differ in predation risk, less is known about the predictability of changes in physiological mechanisms underlying these phenotypic responses to predation pressure. The physiological response to acute and chronic stressors such as predation risk is highly conserv...

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Section: Discussionmentioning

confidence: 99%

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

McGhee

Paitz

Baker

et al. 2020

Sci Rep

Self Cite

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“…The return of all elevated cortisol deposits back to control levels by 48 hpf (hatch) illustrates the importance of maintaining low cortisol levels during this early developmental window. While the mechanism(s) is unclear, a recent study suggested a role for ATP-binding cassette transporters in the rapid cortisol clearance in threespine stickleback ( Gasterosteus aculeatus ) embryos40. Another possibility is the enzyme 11βHSD2, which converts cortisol to inactive cortisone and contains putative glucocorticoid response elements (GRE) in its promoter region41.…”

Section: Discussionmentioning

confidence: 99%

Maternal cortisol stimulates neurogenesis and affects larval behaviour in zebrafish

Best

Kurrasch

Vijayan

2017

Sci Rep

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Excess glucocorticoid transferred from stressed mother to the embryo affects developing vertebrate offspring, but the underlying programming events are unclear. In this study, we tested the hypothesis that increased zygotic glucocorticoid deposition, mimicking a maternal stress scenario, modifies early brain development and larval behaviour in zebrafish (Danio rerio). Cortisol was microinjected into the yolk at one cell-stage, to mimic maternal transfer, and the larvae [96 hours post-fertilization (hpf)] displayed increased activity in light and a reduction in thigmotaxis, a behavioural model for anxiety, suggesting an increased propensity for boldness. This cortisol-mediated behavioural phenotype corresponded with an increase in primary neurogenesis, as measured by incorporation of EdU at 24 hpf, in a region-specific manner in the preoptic region and the pallium, the teleostean homolog of the hippocampus. Also, cortisol increased the expression of the proneural gene neurod4, a marker of neurogenesis, in a region- and development-specific manner in the embryos. Altogether, excess zygotic cortisol, mimicking maternal stress, affects early brain development and behavioural phenotype in larval zebrafish. We propose a key role for cortisol in altering brain development leading to enhanced boldness, which may be beneficial in preparing the offspring to a stressful environment and enhancing fitness.

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“…Cortisol has been detected in both fertilised and unfertilised eggs of numerous species, including white sturgeon Acipenser transmontanus Richardson 1837 (Simontacchi et al, ), Mozambique tilapia Oreochromis mossambicus (Peters 1852) (Hwang & Wu, ), O. mykiss (Auperin & Geslin, ), D. labrax , Japanese flounder Paralichthys olivaceus (Temminck & Schlegel 1846) (de Jesus et al, ), chum salmon Oncorhynchus keta (Walbaum 1792) (de Jesus & Hirano, ), yellow perch Perca flavescens (Mitchill 1814) (Jentoft et al, ) and three‐spinned stickleback Gasterosteus aculeatus (L. 1758) (Paitz et al, ). Owing to inter‐specific variation, the quantity of cortisol in eggs varies between 1 and 600 ng g −1 , as reviewed in Sopinka et al ().…”

Section: Sampling Matrices To Extract Cortisolmentioning

confidence: 99%

“…The regulation probably occurs in ovaries in direct link with the level of 11bHSD2 (Faught et al, ), an enzyme that allows conversion of cortisol to cortisone, its physiologically inert metabolite. Once in the eggs, the cortisol is also actively excreted by the ATP‐binding cassette (ABC) transporters that clears the steroid (Paitz et al, ). The cortisol transmitted from the mother to the offspring was shown to confer positive ( i.e .…”

Section: Sampling Matrices To Extract Cortisolmentioning

confidence: 99%

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Measuring cortisol, the major stress hormone in fishes

Sadoul

Geffroy

2019

Journal of Fish Biology

265

141

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Stress in teleosts is an increasingly studied topic because of its interaction with growth, reproduction, immune system and ultimately fitness of the animal. Whether it is for evaluating welfare in aquaculture, adaptive capacities in fish ecology, or to investigate effects of human‐induced rapid environmental change, new experimental methods to describe stress physiology in captive or wild fish have flourished. Cortisol has proven to be a reliable indicator of stress and is considered the major stress hormone. Initially principally measured in blood, cortisol measurement methods are now evolving towards lower invasiveness and to allow repeated measurements over time. We present an overview of recent achievements in the field of cortisol measurement in fishes, discussing new alternatives to blood, whole body and eggs as matrices for cortisol measurement, notably mucus, faeces, water, scales and fins. In parallel, new analytical tools are being developed to increase specificity, sensitivity and automation of the measure. The review provides the founding principles of these techniques and introduces their potential as continuous monitoring tools. Finally, we consider promising avenues of research that could be prioritised in the field of stress physiology of fishes.

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Stickleback embryos use ATP-binding cassette transporters as a buffer against exposure to maternally derived cortisol

Cited by 25 publications

References 64 publications

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

Effects of predation risk on egg steroid profiles across multiple populations of threespine stickleback

Maternal cortisol stimulates neurogenesis and affects larval behaviour in zebrafish

Measuring cortisol, the major stress hormone in fishes

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