Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin ( Strongylocentrotus purpuratus ) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT 50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting.
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Life stages differ in plasticity to temperature fluctuations and uniquely contribute to adult phenotype
Adaptive thermal plasticity allows organisms to adjust their physiology to cope with fluctuating environments. However, thermal plasticity is rarely studied in response to thermal variability and is often measured in a single life stage. Plasticity in response to thermal variability likely differs from responses to constant temperatures or acute stress. In addition, life stages likely differ in their plasticity and responses in one stage may be affected by the experiences in a previous stage. Increasing the resolution with which we understand thermal plasticity in response to thermal variation across ontogeny is crucial to understanding how organisms cope with the thermal variation in their environment and to estimating the capacity of plasticity to mitigate costs of rapid environmental change. We wanted to know if life stages differ in their capacity for thermal plasticity under temperature fluctuations. We reared Onthophagus taurus dung beetles in either low or high temperature fluctuation treatments and quantified thermal plasticity of metabolism of pupae and adults. We found that adults were thermally plastic and pupae were not. Next, we wanted to know if the plasticity observed in the adult life stage was affected by the thermal conditions during development. We again used low and high temperature fluctuation treatments and reared individuals in one condition through all egg to pupal stages. At eclosion, we switched half of the individuals in each treatment to the opposite fluctuation condition and, later, measured thermal plasticity of metabolism on adults. We found that temperature conditions experienced during the adult stage, but not egg to pupal stages, affects adult thermal plasticity. However, temperature fluctuations during development affect adult body size, suggesting that some aspects of the adult phenotype are decoupled from previous life stages and others are not. Our data demonstrate that life stages mount different responses to temperature variability and uniquely contribute to the adult phenotype. These findings emphasize the need to broadly integrate the life cycle into studies of phenotypic plasticity and physiology; doing so should enhance our ability to predict organismal responses to rapid global change and inform conservation efforts.
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- NSF-PAR ID:
- 10196407
- Date Published:
- Journal Name:
- The Journal of Experimental Biology
- ISSN:
- 0022-0949
- Page Range / eLocation ID:
- jeb.227884
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Although environmental variability and predictability have been proposed as the underlying ecological context in which transgenerational plasticity (
TGP ) arises, the adaptive significance and interaction with within‐generation plasticity (WGP ) in such scenarios is still poorly understood. To investigate these questions, we considered the tolerance to upper thermal limits of larvae and adults of the desert endemicDrosophila mojavensis adapted to different climatic regions (Desert vs. Mediterranean climate).Thermal plasticity was investigated by acclimating parents and offspring at 36°C (vs. at 25°C). We then used historical temperature variation data from both regions to perform individual‐based simulations by modelling expected components of adaptive plasticity in multiple life stages.
Our results indicated that thermal response to ramping heat shocks was more pronounced in larvae, where acclimation treatments in parents and offspring increased their heat‐shock performance, while heat knockdown in adults was only increased by offspring acclimation of adults. The relative contribution of
WGP andTGP was greater for the population from the more thermally variable Sonoran Desert.Similarly, individual‐based simulations of evolving maternal effects indicated that variation in tolerance to upper thermal limits across life stages and climates is expected from its adaptive significance in response to environmental predictability.
Our approach offers a new perspective and interpretation of adaptive plasticity, demonstrating that environmental predictability can drive thermal responses across generations and life stages in a scenario with regional climate variability.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
Environmental variability shapes evolution, plasticity and biogeographic responses to climate changemore » « less
Abstract Aim We examine how environmental variability at seasonal and interannual time‐scales influences evolutionary trajectories and the role of plasticity in response to recent and future climate change at biogeographic scales. We investigate the interplay of selection pressures at chronic (performance) and acute (thermal stress) time‐scales.
Location Colorado, USA.
Time period 1950–2099.
Major taxa studied A montane butterfly, clouded sulphur (
Colias eriphyle W.H. Edwards, 1876).Methods We leverage field and laboratory data to construct phenotype‐based models that predict fitness and evolutionary responses to recent and future climate change. Our focal phenotype, wing solar absorptivity, responds plastically to developmental (pupal) temperatures and determines adult fitness via its influence on body temperature.
Results We project that phenology accelerates with decreasing elevation and climate change, but gradients in pupal and adult temperature with climate change are modest. Fitness of the first generation is predicted to decrease at low elevations and increase at high elevations with warming. Elevational clines in optimal wing absorptivity shift towards lower absorptivities with warming. We project that temporal shifts from selection for wing darkening (to extend flight time) to selection for wing lightening (to avoid overheating) in some cool, montane locations will ultimately impose fitness costs.
Main conclusions Our analysis suggests that shifts in the balance of selection between acute and chronic responses to environmental variation will alter biogeographic responses to climate change. Evolutionary lags may ultimately confer greater sensitivity to climate change, but plasticity can reduce evolutionary lags by facilitating trait evolution.
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Abstract Changes in seasonality associated with climate warming (e.g. temperature, growing season duration) are likely to alter invertebrate prey biomass and availability in aquatic ecosystems through direct and indirect influences on physiology and phenology, particularly in arctic lakes. However, despite warmer thermal regimes, photoperiod will remain unchanged such that potential shifts resulting from longer and warmer growing seasons could be limited by availability of sunlight, especially at lower trophic levels. Thus, a better understanding of warming effects on invertebrate prey throughout the growing season (e.g. early, peak, late) is important to understand arctic lake food‐web dynamics in a changing climate.
Here, we use a multifaceted approach to evaluate prey availability to predators in lakes of arctic Alaska. In a laboratory mesocosm experiment, we measured different metrics of abundance for snails (
Lymnaea elodes ) and zooplankton (Daphnia middendorffiana ) across three time periods (early, mid‐ and late growing season) and across three temperature and photoperiod treatments (control, increased temperature and increased temperature × photoperiod). Additionally, we used generalised additive models and generalised additive mixed‐effects models to relate long‐term empirical observations of zooplankton biomass (1983–2015) to observed temperature regimes in an arctic lake. We then simulated zooplankton biomass for the warmest temperature observations across the growing season to inform likely zooplankton biomass regimes under future change.We observed variable responses by snails and zooplankton across experiments and treatments. Early in the growing season, snail development was accelerated at multiple life stages (e.g. egg and juvenile). In mid‐season, in accordance with warmer temperatures, we observed significantly increased
Daphnia abundances. However, in the late season,Daphnia appeared to be limited by photoperiod. Confirming our experimental results, our models of zooplankton biomass showed an increase of nearly 20% in warmer years. Further, these model estimates could be conservative as the consumptive demand of fishes may increase in warmer years as well.Overall, our results highlight the importance of interactive effects of temperature and seasonality. Based primarily on temperature, we can readily predict the response of fish metabolism in warmer temperatures. However, in this context, we generally require a better understanding of climate‐driven responses of important invertebrate prey resources. Our results suggest invertebrate prey biomass and availability are likely to respond positively with climate change based on temperature and seasonality, as well as proportionally to the metabolic requirements of fish predators. While further research is necessary to understand how other food‐web components will respond climate change, our findings suggest that the fish community at the top of arctic lake food webs will have adequate prey base in a warming climate.
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Exposure to stressful low temperatures during development can result in the accumulation of deleterious physiological effects called chill injury. Metabolic imbalances, disruptions in ion homeostasis, and oxidative stress contribute to the increased mortality of chill-injured insects. Interestingly, survival can be significantly increased when chill susceptible insects are exposed to a daily warm-temperature pulse during chilling. We hypothesize that warm pulses allow for the repair of damage associated with chill-injury. Here, we describe transcriptional responses during exposure to a fluctuating thermal regime (FTR), relative to constant chilled temperatures, during pupal development in the alfalfa leafcutting bee, Megachile rotundata using a combination of RNA-seq and qPCR. Pupae were exposed to either a constant, chilled temperature of 6°C, or 6°C with a daily pulse of 20°C for seven days. RNA-seq after experimental treatment revealed differential expression of transcripts involved in construction of cell membranes, oxidation-reduction and various metabolic processes. These mechanisms provide support for shared physiological responses to chill injury across taxa. The large number of differentially expressed transcripts observed after seven days of treatment suggests that the initial divergence in expression profiles between the two treatments occurred upstream of the time point sampled. Additionally, the differential expression profiles observed in this study show little overlap with those differentially expressed during temperature stress in the diapause state of M. rotundata. While the mechanisms governing the physiological response to low-temperature stress are shared, the specific transcripts associated with the response differ between life stages.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.227884
