Abstract
Phenotypic plasticity describes the ability of an organism with a given genotype to respond to changing environmental conditions through the adaptation of the phenotype. Phenotypic plasticity is a widespread means of adaptation, allowing organisms to optimize fitness levels in changing environments. A core prerequisite for adaptive predictive plasticity is the existence of reliable cues, i.e. accurate environmental information about future selection on the expressed plastic phenotype. Furthermore, organisms need the capacity to detect and interpret such cues, relying on specific sensory signalling and neuronal cascades. Subsequent neurohormonal changes lead to the transformation of phenotype A into phenotype B. Each of these activities is critical for survival. Consequently, anything that could impair an animal’s ability to perceive important chemical information could have significant ecological ramifications. Climate change and other human stressors can act on individual or all of the components of this signalling cascade. In consequence, organisms could lose their adaptive potential, or in the worst case, even become maladapted. Therefore, it is key to understand the sensory systems, the neurobiology and the physiological adaptations that mediate organisms’ interactions with their environment. It is, thus, pivotal to predict the ecosystem-wide effects of global human forcing. This review summarizes current insights on how climate change affects phenotypic plasticity, focussing on how associated stressors change the signalling agents, the sensory systems, receptor responses and neuronal signalling cascades, thereby, impairing phenotypic adaptations.
Zusammenfassung
Die phänotypische Plastizität beschreibt die Fähigkeit eines Organismus mit einem bestimmten Genotyp, auf veränderte Umweltbedingungen durch die Anpassung des Phänotyps zu reagieren. Die phänotypische Plastizität ist ein weit verbreitetes Mittel der Anpassung, das es Organismen ermöglicht, ihre Fitness in einer sich verändernden Umwelt zu optimieren. Eine wesentliche Voraussetzung für die adaptive prädiktive Plastizität ist das Vorhandensein zuverlässiger Hinweise, d. h. genauer Umweltinformationen über die künftige Selektion auf den ausgeprägten plastischen Phänotyp. Darüber hinaus müssen Organismen in der Lage sein, solche Hinweise zu erkennen und zu interpretieren, wobei sie sich auf spezielle sensorische Signalwege und neuronale Kaskaden stützen. Die anschließenden neurohormonellen Veränderungen führen zur Umwandlung von Phänotyp A in Phänotyp B. Jede dieser Aktivitäten ist für das Überleben entscheidend. Folglich könnte alles was die Fähigkeit eines Tieres wichtige chemische Informationen wahrzunehmen beeinträchtigen könnte, erhebliche ökologische Auswirkungen haben. Der Klimawandel und andere menschliche Stressfaktoren können auf einzelne oder alle Komponenten dieser Signalkaskade einwirken. In der Folge könnten Organismen ihr Anpassungspotenzial verlieren oder können im schlimmsten Fall sogar Fehlanpassungen entwickeln. Daher ist es von entscheidender Bedeutung, die sensorischen Systeme, die Neurobiologie und die physiologischen Anpassungen zu verstehen, die die Interaktionen von Organismen mit ihrer Umwelt vermitteln. Es ist daher von zentraler Bedeutung, die Auswirkungen globaler menschlicher Einflüsse auf das gesamte Ökosystem vorherzusagen. Dieser Übersichtsartikel fasst die aktuellen Erkenntnisse darüber zusammen, wie sich der Klimawandel auf die phänotypische Plastizität auswirkt, wobei der Schwerpunkt darauf liegt, wie die damit verbundenen Stressoren die Signalstoffe, die sensorischen Systeme, die Rezeptorantworten und die neuronalen Signalkaskaden verändern und dadurch die phänotypischen Anpassungen beeinträchtigen.
Funding source: Deutsche Forschungsgemeinschaft 10.13039/501100001659
Award Identifier / Grant number: WE6019/2-1
About the author
Linda C. Weiss studied Biology at the Ruhr University Bochum. After receiving her Diploma degree in Neurobiology in 2007 under the supervision of Prof. Dr. K.P. Hoffmann, she started her doctoral degree in 2008 at the Department of Animal Ecology, Evolution and Biodiversity in the lab of Prof. Dr. R. Tollrian. After receiving her Ph.D. in 2011, she moved to the LMU Munich and Christian Laforsch for a guest scientist stay. She obtained a scholarship by the Deutsche Akademie der Naturforscher Leopoldina and joined Prof. Dr. John K. Colbourne’s Environmental Genomics group in Birmingham, UK, as a postdoctoral fellow. Since 2016, she works as a senior group leader at the Ruhr University Bochum. Here, she studies the molecular and neuronal mechanisms underlying phenotypic plasticity in aquatic animals.
Excursion 1: Phenotypic mismatches to environmental conditions
Light is one important factor that tunes the rhythmicity of specific behaviours (e.g. reproduction, migration, (in)activity) to diel, lunar, and seasonal cycles. With opsin and cryptochrome receptors located on special nerve cells, organisms can sense changes in the light (spectral/intensity) and photoperiodic regimes (daily, annual) controlling their chronobiology (Häfker and Tessmar-Raible, 2020). Urbanization-associated light pollution can disrupt this temporal niche use so that organisms are less well-adapted to their environment with consequences for their fitness. For example, the magnitude of circadian clock-controlled diel vertical migration in the freshwater crustacean Daphnia is reduced by nocturnal light (Häfker and Tessmar-Raible, 2020; Moore et al., 2000; Rund et al., 2016). Furthermore, seasonal coat-colour changes in mammals and birds of polar regions are controlled by physiological mechanisms entrained by photoperiod and optimized to match local conditions (Zimova et al., 2018). However, as seasonal duration and extent of snow cover decline through increasing global temperatures, species become colour-mismatched to their environment. In consequence, they lose the advantageous effect of seasonally tuned camouflage (Zimova et al., 2018).
Excursion 2: Pollutants disrupting sensory abilities
It is important to mention that there are also anthropogenic pollutants that can disrupt sensory systems, even at low, non-toxic concentrations (Troyer and Turner, 2015). Heavy metals are known to have toxicological effects on the mechanosensory lateral line system of fish. Being externally located, they are directly exposed to compounds in the surrounding environment and therefore prone to damage. In zebrafish (Danio rerio), for example, the level of damage to the neuromasts depends on the concentration of dissolved copper. Doses above 50 μg/L lead to an almost complete cell death (Kelley et al., 2018; McNeil et al., 2014). Subsequent studies with larval zebra fish have shown that exposure to both copper (CuSO4) and silver (AgNO3) metal salts is associated with a reduction in the number of neuromasts and a failure to orientate in a water current (Kelley et al., 2018; McNeil et al., 2014). Further stressors described include chemicals belonging to the group of antidepressants that enter aquatic systems through waste waters. These pharmaceuticals are designed to interfere with neuronal signalling cascades and thus have a foreseeable but often not described effects on species’ (neuro)-physiology, populations and community structures.
Excursion 3: Further examples of sensory systems prone to climate change
Elevated pCO2 effects have been tested on the capacity of visual detection in larval temperate gobies (Gobiusculus flavescens). The animals show an increase in phototactic activity, suggesting a visual hypersensitivity (Forsgren et al., 2013). Further, the flicker fusion threshold, a capacity important for movement tracking, was found to be reduced in spiny damselfish (Acanthochromis polyacanthus) (Chung et al., 2014). Elevated pCO2 can also directly change auditory sensitivity through an increased otolith size used by fish to detect sound waves (Bignami et al., 2013; Shen et al., 2016). Such a hypersensitivity may impair the ability to discriminate behaviourally relevant auditory cues from ‘background noise’.
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Author contributions: The author has accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: The author gratefully acknowledges the financial support from the Deutsche Forschungsgemeinschaft (WE6019/2-1).
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Conflict of interest statement: The author declares no conflicts of interest regarding this article.
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