Rapid within‐ and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes

Cavieres, Grisel; Rezende, Enrico L.; Clavijo‐Baquet, Sabrina; Alruiz, José M.; Rivera-Rebella, Carla; Boher, Francisca; Bozinovic, Francisco

doi:10.1002/ece3.6496

Cited by 18 publications

(16 citation statements)

References 68 publications

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“…Insects often compensate physiologically to environmental stress through within generation and trans‐generational phenotypic plasticity (Whitman, 2009; Sgrò et al ., 2016; Cavieres et al ., 2020). Moreover, for co‐occurring environmental stressors, organisms often share physiological mechanisms—cross‐tolerance or signal pathways—cross‐talk (Sinclair et al ., 2013; Pallarés et al ., 2017; Gotcha et al ., 2018).…”

Section: Introductionmentioning

confidence: 99%

Desiccation and temperature resistance of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae): pedestals for invasion success?

Mutamiswa

Machekano

Singano³

et al. 2021

Physiol. Entomol.

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The larger grain borer, Prostephanus truncatus (Horn) is an invasive insect pest species of global economic concern. It however remains unknown how P. truncatus succeeds under increasing temperatures and desiccation effects associated with projected climate change. Here, we investigated the effects of desiccation and high‐temperature stress on physiological fitness of P. truncatus larvae and adults. Specifically, we measured critical thermal maxima, heat knockdown time and water loss rates following heat and desiccation acclimation. Results showed beneficial heat acclimation effects on heat tolerance (critical thermal maxima and heat knockdown time). Similarly, desiccation acclimation significantly improved both heat tolerance traits, indicating cross‐tolerance effects, not for heat knockdown time in larvae. In all cases, adults exhibited more improved heat tolerance than larvae. Conversely, heat acclimation increased water loss rates, and more so in larvae than adults. Improved heat tolerance plus abiotic stress cross‐tolerance of P. truncatus may explain its enhanced physiological and ecological fitness in dry tropical and changing climate environments. These results are important in explaining the role of physiology in insect invasions and may inform pest management and forecasting.

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Section: Introductionmentioning

confidence: 99%

Desiccation and temperature resistance of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae): pedestals for invasion success?

Mutamiswa

Machekano

Singano³

et al. 2021

Physiol. Entomol.

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“…Similarly, diurnal fluctuations exacerbated the effects of temperature in reducing fathead minnows Pimephales promelas size, compared to constant warming, despite having beneficial effects on their upper thermal tolerance limits (Salinas, Irvine, Schertzing, Golden, & Munch, 2019). Notably, in the fruit fly Drosophila melanogaster , the same increased thermal tolerance provided by temperature fluctuations was however accompanied by fitness and reproductive costs, such as lower fecundity and reproductive output (Cavieres et al, 2020). Yet, since we lack a non-fluctuating treatment within our experiment, we cannot rule out the possibility that the differences between this and previous studies are due to other factors, and not the diel fluctuation in temperature.…”

Section: Discussionmentioning

confidence: 99%

Timing specific parental effects of ocean warming in a coral reef fish

Bonzi,

Spinks,

Donelson

et al. 2023

Preprint

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Population and species persistence in a rapidly warming world will be determined by an organisms’ ability to acclimate to warmer conditions, especially across generations. There is potential for transgenerational acclimation, but the importance of ontogenetic timing in the transmission of environmentally induced parental effects remains mostly unknown. We aimed to disentangle the contributions of two critical ontogenetic stages (juvenile development and adult reproduction) to transgenerational plasticity, by exposing the coral reef fishAcanthochromis polyacanthusto simulated ocean warming with natural diel thermal fluctuations across two generations. By using hepatic transcriptomics, we discovered that the developmental environment of the offspring themselves had little effect on their acclimation potential at 2.5 months of life. Instead, the developmental experience of parents increased regulatory RNA production and protein synthesis, which could improve the offspring’s response to warming. Conversely, reproduction in warmer water elicited stress response mechanisms, with suppression of translation and mitochondrial respiration. Mismatches between temperatures in the parental ontogenetic thermal experience deeply affected offspring gene expression profiles, and detrimental effects were also evident when warming occurred both during parents’ development and reproduction. This study reveals that the previous generation’s developmental temperature contributes substantially to thermal acclimation potential during early life, however prolonged heat stress will likely have adverse effects on the species’ persistence.

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“…Most importantly, our results suggest that P. incisus may evolve rapidly and complete TGP to MHW, with full amelioration of its lethal effect in the second generation. The transgenerational plasticity of MHWs comes with a cost of reduced reproduction, and grazing may be a crucial and widespread mechanism for marine invertebrates coping with the transient effects of heatwaves (Cavieres et al, 2020 ; Dinh et al, 2020 ; Doan et al, 2019 ). Interestingly, fish predator cues played a minor role in shaping both immediate and transgenerational effects of MHWs, highlighting the dominant effects of MHWs on P. incisus .…”

Section: Discussionmentioning

confidence: 99%

Transgenerational exposure to marine heatwaves ameliorates the lethal effect on tropical copepods regardless of predation stress

Truong

Doan

et al. 2022

Ecology and Evolution

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Marine heatwaves (MHWs) are emerging as a severe stressor in marine ecosystems. Extreme warm sea surface temperatures during MHWs often exceed the optimal thermal range for more than one generation of tropical coastal zooplankton. However, it is relatively unknown whether transgenerational plasticity (TGP) to MHWs may shape the offspring's fitness, particularly in an ecologically relevant context with biotic interactions such as predation stress. We addressed these novel research questions by determining the survival, reproductive success, and grazing rate of the copepod Pseudodiaptomus incisus exposed to MHW and fish predator cues (FPC) for two generations (F1 and F2). The experiment was designed in a full orthogonal manner with 4 treatments in F1 and 16 treatments in F2 generation. In both generations, MHW reduced P. incisus survival, reproductive parameters, and grazing by 10%–62% in MHW, but these parameters increased by 2%–15% with exposure to FPC, particularly at control temperature. F2 reproductive success and grazing rate as indicated by cumulative fecal pellets were reduced by 20%–30% in F1‐MHW, but increased by ~2% in F1‐FPC. Strikingly, MHW exposure reduced 17%–18% survival, but transgenerational exposure to MHWs fully ameliorated its lethal effect and this transgenerational effect was independent of FPC. Increased survival came with a cost of reduced reproductive success, constrained by reduced grazing. The rapid transgenerational MHW acclimation and its associated costs are likely widespread and crucial mechanisms underlying the resilience of coastal tropical zooplankton to MHWs in tropical coastal marine ecosystems.

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Rapid within‐ and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes

Cited by 18 publications

References 68 publications

Desiccation and temperature resistance of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae): pedestals for invasion success?

Desiccation and temperature resistance of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae): pedestals for invasion success?

Timing specific parental effects of ocean warming in a coral reef fish

Transgenerational exposure to marine heatwaves ameliorates the lethal effect on tropical copepods regardless of predation stress

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