Reduced physiological plasticity in a fish adapted to stable temperatures

Morgan, Rachael; Andreassen, Anna H.; Åsheim, Eirik Ryvoll; Finnøen, Mette Helene; Dresler, Gunnar; Brembu, Tore; Loh, Adrian; Miest, Joanna J.; Jutfelt, Fredrik

doi:10.1073/pnas.2201919119

Cited by 74 publications

(50 citation statements)

References 89 publications

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“…We hypothesised that (i) the metabolomic profiles excreted by control and heat-stressed zebrafish embryos differ from each other; (ii) there may be similarities between the transcriptomic signatures of embryos exposed to heat stress and to stress metabolites, including in the response of chemosensory perception genes, and (iii) both heat-stressed and indirectly stressed individuals differ in growth patterns and behaviour from controls. (iv) Laboratory strains of zebrafish may perform differently to their wild counterparts (29), and embryos in clutches may react differently than single embryos in tubes. We expected to find similar molecular responses to stress metabolites in group-raised outcrossing zebrafish embryos, but perhaps with different magnitudes.…”

Section: Introductionmentioning

confidence: 99%

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Feugere

Bates

Emagbetere

et al. 2022

Preprint

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Heat alters biology from molecular to ecological levels, but may also have unknown indirect effects. This includes the novel concept that animals exposed to abiotic stress can induce stress in naive receivers. Here, we provide a comprehensive picture of the molecular signatures of this process, by integrating multi-omic and phenotypic data. In individual zebrafish embryos, repeated heat peaks elicited both a molecular response and a burst of accelerated growth followed by a growth slow-down in concert with reduced responses to novel stimuli. Metabolomes of the media of heat treated vs. untreated embryos revealed candidate stress metabolites including sulphur-containing compounds and lipids. These stress metabolites elicited transcriptomic changes in naive receivers related to immune response, extracellular signalling, glycosaminoglycan/keratan sulphate, and lipid metabolism. Consequently, non heat-exposed receivers (exposed to stress metabolites only) experienced accelerated catch-up growth in concert with reduced swimming performance. The combination of heat and stress metabolites accelerated development the most, mediated by apelin signalling. Our results prove the concept of indirect heat-induced stress propagation towards naive receivers, inducing phenotypes comparable to those resulting from direct heat exposure, but utilising distinct molecular pathways. Group-exposing a non-laboratory zebrafish line, we independently confirm that the glycosaminoglycan biosynthesis-related gene chs1, and the mucus glycoprotein gene prg4a, functionally connected to the candidate stress metabolite classes sugars and phosphocholine, are differentially expressed in receivers. This hints at production of Schreckstoff-like cues in receivers, leading to further stress propagation within groups, which may have ecological and animal welfare implications for aquatic populations in a changing climate.Significance StatementAquatic animals utilise chemicals to mediate adaptive behaviours. For instance, predated fish release chemical cues that elicit antipredatory responses in naive receivers. But whether abiotic factors such as heat likewise alter chemical communication has received little focus. Here, we uncover a novel dimension of chemical communication — heat-stressed donors can induce stress in naive receivers. We show that heat activates molecular stress responses, leading to the release of distinct stress metabolite classes into the environment. These stress metabolites alter the transcriptome of receivers, resulting in faster development and hypoactivity. Heat combined with stress metabolites had the largest effect, highlighting that abiotic stress, experienced both directly and indirectly, can alter chemical communication and affect embryonic development.Graphical AbstractHighlightsWe elucidate the mechanism for a novel dimension of the heat stress response — chemical communication from heat-stressed donors that induces stress in naive receivers — constituting a positive feedback loopRepeated heat stress induces a cellular and cortisol stress response and alters the phenotype of zebrafish embryosHeat-stressed embryos release stress metabolites enriched in lipids and sulphur-containing organo-oxygen compoundsIn combination, heat and stress metabolites induced 47% distinct differentially expressed genes, with many related to organ developmentThese stress metabolites alter the transcriptome and induce both faster development and hypoactivity in naive receivers, a similar response to that of heat stress itself

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Section: Introductionmentioning

confidence: 99%

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Feugere

Bates

Emagbetere

et al. 2022

Preprint

View full text Add to dashboard Cite

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“…S1), and this variability could play an important role in shaping species’ responses to change ( 3 ). For example, variable environments could select for plasticity ( 47 ) with implications for adaptation ( 48 ). Future work assessing how different temporal scales of environmental variability (i.e., diel, semidiel, and seasonal) or predictability alter species’ performance will help to further elucidate the role of variability in structuring evolutionary responses to global change.…”

Section: Discussionmentioning

confidence: 99%

Population-specific vulnerability to ocean change in a multistressor environment

et al. 2023

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Variation in environmental conditions across a species’ range can alter their responses to environmental change through local adaptation and acclimation. Evolutionary responses, however, may be challenged in ecosystems with tightly coupled environmental conditions, where changes in the covariance of environmental factors may make it more difficult for species to adapt to global change. Here, we conduct a 3-month-long mesocosm experiment and find evidence for local adaptation/acclimation in populations of red sea urchins, Mesocentrotus franciscanus , to multiple environmental drivers. Moreover, populations differ in their response to projected concurrent changes in pH, temperature, and dissolved oxygen. Our results highlight the potential for local adaptation/acclimation to multivariate environmental regimes but suggest that thresholds in responses to a single environmental variable, such as temperature, may be more important than changes to environmental covariance. Therefore, identifying physiological thresholds in key environmental drivers may be particularly useful for preserving biodiversity and ecosystem functioning.

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“…The process of adaptation to stable temperature environments has been experimentally shown to limit physiological plasticity in response to future changes to those temperatures (Morgan et al . 2022).…”

Section: Discussionmentioning

confidence: 99%

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

Rivera‐Colón¹,

Rayamajhi²,

Minhas³

et al. 2022

Preprint

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White-blooded Antarctic icefishes are an example of extreme biological specialization to both the chronic cold of the Southern Ocean and life without hemoglobin. As a result, icefishes display derived physiology that limits them to the cold and highly oxygenated Antarctic waters. Against these constraints, remarkably one species, the pike icefish Champsocephalus esox, successfully colonized temperate South American waters. To study the genetic mechanisms underlying secondarily temperate adaptation of C. esox, we generated chromosome-level genome assemblies of both C. esox and its Antarctic sister species, Champsocephalus gunnari. The C. esox genome is similar in structure and organization to that of its Antarctic congener; however, we observe evidence of chromosomal rearrangements coinciding with regions of elevated genetic divergence in pike icefish populations. We also find several key biological pathways under selection, including genes related to mitochondria and vision, highlighting candidates behind temperate adaptation in C. esox. Substantial antifreeze glycoprotein (AFGP) pseudogenization has occurred in the pike icefish, likely due to relaxed selection following ancestral escape from Antarctica. The canonical AFGP locus organization is conserved in C. esox and C. gunnari, but both show a translocation of two AFGP copies to a separate locus, previously unobserved in cryonotothenioids. Our study presents the first whole genome characterization of a secondarily temperate notothenioid to date, providing a key resource and platform for understanding the adaptive potential of the highly vulnerable icefishes, and of cryonotothenioids in general, in face of a warming Antarctic environment.

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Reduced physiological plasticity in a fish adapted to stable temperatures

Cited by 74 publications

References 89 publications

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Population-specific vulnerability to ocean change in a multistressor environment

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

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