Are ectotherm brains vulnerable to global warming?

doi:10.1016/j.tree.2021.04.009

Trends in Ecology & Evolution

Volume 36, Issue 8, August 2021, Pages 691-699

https://doi.org/10.1016/j.tree.2021.04.009 Get rights and content

Highlights

Ectotherm brains are remarkably plastic to changes in developmental temperature; however, their physiological requirements may still make them susceptible to the higher temperatures associated with global warming.
Global warming affects the development of the ectotherm brain because rising temperature stimulate neuronal activity and growth up to a certain threshold, above which it is detrimental to neuron development.
Making predictions about temperature effects on neuronal development and cognition is currently hampered by what might be highly taxon-dependent effects documented in a limited number of species.
We propose that studying the developmental plasticity of the ectotherm brain can help us predict how a wider range of species will respond to global warming.

Elevated temperatures during development affect a wide range of traits in ectotherms. Less well understood is the impact of global warming on brain development, which has only rarely been studied experimentally. Here, we evaluate current progress in the field and search for common response patterns among ectotherm groups. Evidence suggests that temperature may have a positive effect on neuronal activity and growth in developing brains, but only up to a threshold, above which temperature is detrimental to neuron development. These responses appear to be taxon dependent but this assumption may be due to a paucity of data for some taxonomic groups. We provide a framework with which to advance this highly promising field in the future.

Section snippets

Elevated temperatures affect ectotherm development

While elevated temperatures have been shown to affect a wide range of phenotypic traits [1,2] (Box 1), the impact of global warming on brain development has only recently been addressed. The brain was once thought to be a static organ due to its crucial role in controlling important physiological and behavioral processes [3]. However, we now know that brain development is a plastic, self-organizing process affected by a wide range of external factors including stress, diet, and importantly,

Common effects of elevated developmental temperatures on ectotherm brains

We conducted a literature search of studies that performed incubation of embryos and reported changes in the brain extending after birth (Figure 1; see supplemental information online). Overall, it is difficult to make generic statements on the responses to high temperature on the developing ectotherm brain because the reported effects depend on which baseline or control temperatures are tested and thus, how response curves are constructed. Therefore, ecological consequences will crucially

Predictions for a warmer future

Currently, we have little understanding of what the key variables are that determine how ectotherm brain development responds to temperature. The study of the role of developmental temperatures in ectotherm brains is challenging because of their incredible diversity of ectotherms and the wide range of life histories they exhibit. Also, importantly, we are constrained by a lack of experimental standardization in the field and a dearth of experimental studies that generally lack ecological

Framework for future studies

The lack of experimental standards has complicated the understanding of temperature-induced changes in the developing brain of ectotherms. We provide some basic guidelines to ensure that further research provides comparable findings across taxa and facilitates future metanalyses.

Concluding remarks

Research to date shows that the brains of ectotherms have a remarkably plastic response to changes in developmental temperature. Importantly, the effect of rising temperatures is not a linear, universal response but rather the consequence of physiological changes that depends on the starting temperature [9]. For instance, increasing developmental temperatures up to 30°C enhances cognitive abilities in honeybees, sharks, and some lizards, but higher temperatures disrupt the reproductive

Acknowledgments

We are grateful to two anonymous reviewers for the helpful comments which improved the manuscript. Financial support for this research was provided by Macquarie University. Barry Sinervo sadly passed away on 15 March 2021 while the article was in review. His contribution to this paper, and more generally to evolutionary biology, was immense and will always be remembered.

Declaration of interests

The authors declare no interests.

Glossary

Aromatase: an enzyme that catalyzes the conversion of testosterone to estradiol, which then binds to nuclear and membrane-bound estrogen receptors in various target tissues to exert genomic and non-genomic effects.
Developmental plasticity: the process by which a genotype produces distinct phenotypes depending on the environmental conditions under which development takes place.
Ectothermic animals: animals that derive the heat they require for body functioning from external sources, such as sunlight or

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Climate change increasingly influences the loss of biodiversity, especially in ectothermic organisms, which depend on environmental temperatures to obtain heat and regulate their life cycle. Studies that aim to understand the impact of temperature variation are important to better understand the possible impacts generated on the homeostasis of ectothermic organisms. Our objective was to characterize the responses of juvenile Liolaemus arambarensis lizards to abrupt changes in temperature, quantifying markers of body condition, intermediary and hormonal metabolism and oxidative balance. We collected 45 juvenile individuals of L. arambarensis (winter: 20 and summer: 25) in Barra do Ribeiro, Brazil. We transported the animals to the laboratory, where they were acclimatized for five days at a temperature of 20 °C, then divided and exposed to temperatures of 10 °C, 20 °C, 30 °C and 40 °C for 24 h. After exposure, the animals were euthanized and the brain, caudal muscle, thigh, and liver tissues were extracted for quantification of biomarkers of metabolism (glycogen and total proteins) and oxidative balance (acetylcholinesterase, superoxide dismutase, catalase, glutathione-S-transferase and lipoperoxidation) and plasma for corticosterone quantification. The results show that L. arambarensis is susceptible to sudden temperature variations, where higher temperatures caused greater activity of antioxidant enzymes, increased lipoperoxidation and higher plasma levels of corticosterone in animals eliminated in winter. The present study demonstrated that abrupt changes in temperature could significantly modify the homeostatic mechanisms of animals, which could lead to oxidative stress and a potential trade-off between survival and growth/reproduction. In this context, the organism mobilizes energy resources for survival, with possible damage to growth and reproduction. Demonstrate that a change in temperature can be a potential factor in extinction for a species given the profile of global climate change.
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Global warming is rapidly changing the phenology, distribution, behaviour and demography of wild animal populations. Recent studies in wild animals have shown that high temperatures can induce short-term cognitive impairment, and captive studies have demonstrated that heat exposure during early development can lead to long-term cognitive impairment. Given that cognition underpins behavioural flexibility and can be directly linked to fitness, understanding how high temperatures during early life might impact adult cognitive performance in wild animals is a critical next step to predict wildlife responses to climate change. Here, we investigated the relationship between temperatures experienced during development, adult cognitive performance, and reproductive success in wild southern pied babblers (Turdoides bicolor). We found that higher mean daily maximum temperatures during nestling development led to long-term cognitive impairment in associative learning performance, but not reversal learning performance. Additionally, a higher number of hot days (exceeding 35.5 °C, temperature threshold at which foraging efficiency and offspring provisioning decline) during post-fledging care led to reduced reproductive success in adulthood. We did not find evidence that low reproductive success was linked to impaired associative learning performance: associative learning performance was not related to reproductive success. In contrast, reversal learning performance was negatively related to reproductive success in breeding adults. This suggests that reproduction can carry a cost in terms of reduced performance in cognitively demanding tasks, confirming previous evidence in this species. Taken together, these findings indicate that naturally occurring high temperatures during early development have long-term negative effects on cognition and reproductive success in wild animals. Compounding effects of high temperatures on current nestling mortality and on the long-term cognitive and reproductive performance of survivors are highly concerning given ongoing global warming.
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Anthropogenically driven climate change is predicted to increase average sea surface temperatures, as well as the frequency and intensity of marine heatwaves in the future. This increasing temperature is predicted to have a range of negative physiological impacts on multiple life-stages of coral reef fish. Nevertheless, studies of early-life stages remain limited, and tissue-specific transcriptomic studies of post-larval coral reef fish are yet to be conducted. Here, in an aquaria-based study we investigate the tissue-specific (brain, liver, muscle, and digestive tract) transcriptomic response of post-larval (20 dph) Amphiprion ocellaris to temperatures associated with future climate change (+3 °C). Additionally, we utilized metatranscriptomic sequencing to investigate how the microbiome of the digestive tract changes at +3 °C. Our results show that the transcriptional response to elevated temperatures is highly tissue-specific, as the number of differentially expressed genes (DEGs) and gene functions varied amongst the brain (102), liver (1785), digestive tract (380), and muscle (447). All tissues displayed DEGs associated with thermal stress, as 23 heat-shock protein genes were upregulated in all tissues. Our results indicate that post-larval clownfish may experience liver fibrosis-like symptoms at +3 °C as genes associated with extracellular matrix structure, oxidative stress, inflammation, glucose transport, and metabolism were all upregulated. We also observe a shift in the digestive tract microbiome community structure, as Vibrio sp. replace Escherichia coli as the dominant bacteria. This shift is coupled with the dysregulation of various genes involved in immune response in the digestive tract. Overall, this study highlights post-larval clownfish will display tissue-specific transcriptomic responses to future increases in temperature, with many potentially harmful pathways activated at +3 °C.
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The transition from larval to adult locomotion in the anuran, Xenopus laevis, involves a dramatic switch from axial to appendicular swimming including intermediate stages when the tail and hindlimbs co-exist and contribute to propulsion. Hatchling tadpole swimming is generated by an axial central pattern generator (CPG) which matures rapidly during early larval life. During metamorphosis, the developing limbs are controlled by a de novo appendicular CPG driven initially by the axial system before segregating to allow both systems to operate together or independently. Neuromodulation plays important roles throughout, but key modulators switch their effects from early inhibitory influences to facilitating locomotion. Temperature affects the construction and operation of locomotor networks and global changes in environmental temperature place aquatic poikilotherms, like amphibians, at risk. The locomotor control strategy of anurans differs from other amphibian groups such as salamanders, where evolution has acted upon the thyroid hormone pathway to sculpt different developmental outcomes.
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Citation Excerpt :
This damage is often caused by the denaturing of proteins, oxidative stress, and higher aerobic demand (Beltrán et al., 2021). To prevent or limit this damage, heat shock proteins are produced, and are used to prevent further protein degradation (Beltrán et al., 2021; Iwama et al., 1998). One study conducted on rainbow trout found that there was significant changes in the abundance of many gene transcripts involved in various processes, including neurogenesis, apoptosis, oxidative stress and heat shock protein synthesis (Topal et al., 2021).
Climate change is a growing global issue with many countries and institutions declaring a climate state of emergency. Excess CO₂ from anthropogenic sources and changes in land use practices are contributing to many detrimental changes, including increased global temperatures, ocean acidification and hypoxic zones along coastal habitats. All senses are important for aquatic animals, as it is how they can perceive and respond to their environment. Some of these environmental challenges have been shown to impair their sensory systems, including the olfactory, visual, and auditory systems. While most of the research is focused on how ocean acidification affects olfaction, there is also evidence that it negatively affects vision and hearing. The effects that temperature and hypoxia have on the senses have also been investigated, but to a much lesser extent in comparison to ocean acidification. This review assembles the known information on how these anthropogenic challenges affect the sensory systems of fishes, but also highlights what gaps in knowledge remain with suggestions for immediate action.
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View all citing articles on Scopus

^@: Twitter: @IvanBeltran31 (I. Beltrán), @suzanahh (S. Herculano-Houzel), and @lizard_lab (M.J. Whiting).

^†: Deceased

View full text

Trends in Ecology & Evolution

OpinionAre ectotherm brains vulnerable to global warming?

Highlights

Section snippets

Elevated temperatures affect ectotherm development

Common effects of elevated developmental temperatures on ectotherm brains

Predictions for a warmer future

Framework for future studies

Concluding remarks

Acknowledgments

Declaration of interests

Glossary

Gen. Comp. Endocrinol.

Chemosphere

Gen. Comp. Endocrinol.

Front. Neuroendocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol.

Behav. Process.

Gen. Comp. Endocrinol.

J. Therm. Biol.

Comp. Biochem. Physiol. B Biochem. Mol. Biol.

J. Therm. Biol.

Biol. Conserv.

Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory

PLoS Biol.

Temperature-induced developmental plasticity in ectotherms

Linked regularities in the development and evolution of mammalian brains

Science

Brain evolution and development: adaptation, allometry and constraint

Proc. R. Soc. B Biol. Sci.

Ecological and evolutionary responses to recent climate change

Annu. Rev. Ecol. Evol. Syst.

A global synthesis of animal phenological responses to climate change

Nat. Clim. Chang.

Technical summary

Future of the human climate niche

Proc. Natl. Acad. Sci.

Proteostasis collapse is a driver of cell aging and death

Proc. Natl. Acad. Sci.

Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO2 and warming

Mar. Biol.

Loggerhead sea turtle embryos (Caretta caretta) regulate expression of stress response and developmental genes when exposed to a biologically realistic heat stress

Mol. Ecol.

Growth at cold temperature increases the number of motor neurons to optimize locomotor function

Curr. Biol.

Brain gene expression is influenced by incubation temperature during leopard gecko (Eublepharis macularius) development

J. Exp. Zool. B Mol. Dev. Evol.

FoxK1 splice variants show developmental stage-specific plasticity of expression with temperature in the tiger pufferfish

J. Exp. Biol.

Shrinking body size as an ecological response to climate change

Nat. Clim. Chang.

The effects of incubation temperature on the development of the cortical forebrain in a lizard

Anim. Cogn.

Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development

Proc. Natl. Acad. Sci.

Thermal disruption of mushroom body development and odor learning in Drosophila

PLoS ONE

Daily thermal fluctuations experienced by pupae via rhythmic nursing behavior increase numbers of mushroom body microglomeruli in the adult ant brain

Front. Behav. Neurosci.

Temperature-induced stress response in Lymantria dispar neurosecretory neurons

Turk. J. Biol.

Profiling expression changes of genes associated with temperature and sex during high temperature-induced masculinization in the Nile tilapia brain

Physiol. Genomics

Influence of water temperature on acetylcholinesterase activity in the Pacific tree frog (Hyla regilla)

Environ. Toxicol. Chem.

Opinion
Are ectotherm brains vulnerable to global warming?

Neuro-oxidative damage and aerobic potential loss of sharks under elevated CO₂ and warming