Reversibility of developmental heat and cold plasticity is asymmetric and has long lasting consequences for adult thermal tolerance

Slotsbo, Stine; Schou, Mads Fristrup; Kristensen, Torsten Nygaard; Loeschcke, Volker; Sørensen, Jesper Givskov

doi:10.1242/jeb.143750

Cited by 42 publications

(52 citation statements)

References 47 publications

(63 reference statements)

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“…The thermal limits were assayed at age 3-5 days. During this age span, only very small adjustments of the critical thermal limits are observed (Slotsbo et al 2016). CT min and CT max were estimated in 20 males for each species and each developmental acclimation temperature.…”

Section: T H E R M a L L I M I T Smentioning

confidence: 99%

Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance

et al. 2016

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Summary Thermal limits of ectotherms have been studied extensively and are believed to be evolutionarily constrained, leaving ectotherms at risk under future climate change. Phenotypic plasticity may extend the thermal limits, but we lack detailed characterizations of thermal limit reaction norms as well as an understanding of the interspecific variation in these reaction norms. Here, we investigated the interspecific variation in phenotypic plasticity of thermal limits in 13 Drosophila species. We obtained high‐resolution reaction norms for upper and lower thermal limits across the permissive developmental thermal range (12·5–30 °C). The estimated phenotypes were then associated (while accounting for phylogeny) with climatic parameters from the species’ distributional range. All species showed linear reaction norms for cold tolerance (CTmin) and heat tolerance (CTmax) across developmental acclimation temperatures. We observed strong beneficial cold acclimation to lower temperatures in all species. Conversely, the heat acclimation response was non‐existent in some species, and decreasing or increasing with increasing developmental acclimation temperatures in other species. The degree of phenotypic plasticity of CTmin and CTmax was related neither to the basal thermal limits (trade‐off hypothesis) nor to climatic parameters connected to latitudinal distributions (latitudinal hypothesis). A substantial and linear developmental plasticity of lower thermal limits is a general characteristic of Drosophila species, which allows for straightforward application in species distribution models. In general, upper thermal limits also show linear norms of reaction, but their adaptive significance is limited and highly variable among species, making general predictions across species rather impossible. High‐resolution estimates of norms of reaction of thermal limits can considerably increase our understanding of the capacity of ectotherms to acclimate to different thermal environments. However, our understanding of the environmental drivers of the evolution of phenotypic plasticity and thus of the interspecific differences remains ambiguous, potentially constrained by limited microclimate information. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12782/suppinfo is available for this article.

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Section: T H E R M a L L I M I T Smentioning

confidence: 99%

Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance

et al. 2016

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“…A likely confounding factor in these experiments is the physiological ages of the acclimated versus nonacclimated individuals. Temperature is a significant factor influencing the rate of maturation and ageing in D. melanogaster (Alpatov & Pearl 1929;Blake, Hoopengardner, Centurion, & Helfand, 1996;Bowler & Terblanche, 2008;Slotsbo, Schou, Kristensen, Loeschcke, & Sørensen, 2016), and thus flies subjected to cold acclimation were physiologically younger than their nonacclimated counterparts. Whereas our design does not allow us to make direct statistical comparisons between experiments, we note that the climbing performance of 25°C flies in the acclimation experiment (Figure 4), which were 16-18 days old, was lower than control flies from other experiments (Figures 2 and 3), which were younger (6-8 days old).…”

Section: Discussionmentioning

confidence: 99%

Cold stress results in sustained locomotor and behavioral deficits in Drosophila melanogaster

Garcia

Teets

2019

J Exp Zool Pt A

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Tolerance of climatic stressors is an important predictor of the current distribution of insect species, their potential to invade new environments, and their responses to rapid climate change. Cold stress causes acute injury to nerves and muscles, and here we tested the hypothesis that low temperature causes sublethal deficits in locomotor behaviors that are dependent on neuromuscular function. To do so, we applied a previously developed assay, the rapid iterative negative geotaxis (RING) assay, to investigate behavioral consequences of cold stress in Drosophila melanogaster. The RING assay allows for rapid assessment of negative geotaxis behavior by quantifying climbing height and willingness to climb after cold stress. We exposed flies to cold stress at 0°C and assessed the extent to which duration of cold stress, recovery time, and cold acclimation influenced climbing performance. There was a clear dose‐response relationship between cold exposure and performance deficits, with climbing height and willingness decreasing as cold exposure increased from 2 to 24 hr. Following cold exposure of an intermediate duration (12 hr), climbing height and willingness gradually improved as recovery time increased from 4 to 72 hr but flies never fully recovered. Finally, cold acclimation improved overall climbing height and willingness in both untreated and cold‐stressed flies but did not prevent a reduction in climbing performance. Thus, cold stress causes deficits in locomotor and behavior that are dependent on the dose of cold exposure and persist long after the stress subsides. These results likely have implications for the ecological and evolutionary responses of insect populations to thermally variable environments.

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“…In our experiment, daily temperatures varied between 22.3 and 30.2°C, which exceeds Venturia's adult thermal tolerance (Spanoudis & Andreadis, ). Thermal acclimation during juvenile development could have increased thermal tolerance at the adult stage by reducing the costs of exposure to harmful temperatures in adults (Colinet et al, ; Slotsbo, Schou, Kristensen, Loeschcke, & Sorensen, ), but is unlikely to have prolonged adult life span further than under constant temperature as thermal acclimation is energetically costly (Krebs & Feder, ).…”

Section: Discussionmentioning

confidence: 99%

Environmental degradation amplifies species’ responses to temperature variation in a trophic interaction

Mugabo

Gilljam

Petteway

et al. 2019

Journal of Animal Ecology

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Land‐use and climate change are two of the primary drivers of the current biodiversity crisis. However, we lack understanding of how single‐species and multispecies associations are affected by interactions between multiple environmental stressors.We address this gap by examining how environmental degradation interacts with daily stochastic temperature variation to affect individual life history and population dynamics in a host–parasitoid trophic interaction, using the Indian meal moth, Plodia interpunctella, and its parasitoid wasp Venturia canescens.We carried out a single‐generation individual life‐history experiment and a multigeneration microcosm experiment during which individuals and microcosms were maintained at a mean temperature of 26°C that was either kept constant or varied stochastically, at four levels of host resource degradation, in the presence or absence of parasitoids.At the individual level, resource degradation increased juvenile development time and decreased adult body size in both species. Parasitoids were more sensitive to temperature variation than their hosts, with a shorter juvenile stage duration than in constant temperatures and a longer adult life span in moderately degraded environments. Resource degradation also altered the host's response to temperature variation, leading to a longer juvenile development time at high resource degradation. At the population level, moderate resource degradation amplified the effects of temperature variation on host and parasitoid populations compared with no or high resource degradation and parasitoid overall abundance was lower in fluctuating temperatures. Top‐down regulation by the parasitoid and bottom‐up regulation driven by resource degradation contributed to more than 50% of host and parasitoid population responses to temperature variation.Our results demonstrate that environmental degradation can strongly affect how species in a trophic interaction respond to short‐term temperature fluctuations through direct and indirect trait‐mediated effects. These effects are driven by species differences in sensitivity to environmental conditions and modulate top‐down (parasitism) and bottom‐up (resource) regulation. This study highlights the need to account for differences in the sensitivity of species’ traits to environmental stressors to understand how interacting species will respond to simultaneous anthropogenic changes.

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Reversibility of developmental heat and cold plasticity is asymmetric and has long lasting consequences for adult thermal tolerance

Cited by 42 publications

References 47 publications

Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance

Linear reaction norms of thermal limits in Drosophila: predictable plasticity in cold but not in heat tolerance

Cold stress results in sustained locomotor and behavioral deficits in Drosophila melanogaster

Environmental degradation amplifies species’ responses to temperature variation in a trophic interaction

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