Rapid transgenerational acclimation of a tropical reef fish to climate change (original) (raw)
Related papers
Reproductive Acclimation to Increased Water Temperature in a Tropical Reef Fish
PLoS ONE, 2014
Understanding the capacity of organisms to cope with projected global warming through acclimation and adaptation is critical to predicting their likely future persistence. While recent research has shown that developmental acclimation of metabolic attributes to ocean warming is possible, our understanding of the plasticity of key fitness-associated traits, such as reproductive performance, is lacking. We show that while the reproductive ability of a tropical reef fish is highly sensitive to increases in water temperature, reproductive capacity at +1.5uC above present-day was improved to match fish maintained at present-day temperatures when fish complete their development at the higher temperature. However, reproductive acclimation was not observed in fish reared at +3.0uC warmer than present-day, suggesting limitations to the acclimation possible within one generation. Surprisingly, the improvements seen in reproduction were not predicted by the oxygen-and capacity-limited thermal tolerance hypothesis. Specifically, pairs reared at +1.5uC, which showed the greatest capacity for reproductive acclimation, exhibited no acclimation of metabolic attributes. Conversely, pairs reared at +3.0uC, which exhibited acclimation in resting metabolic rate, demonstrated little capacity for reproductive acclimation. Our study suggests that understanding the acclimation capacity of reproductive performance will be critically important to predicting the impacts of climate change on biological systems.
Molecular Ecology, 2018
Global warming will have far-reaching consequences for marine species over coming decades, yet the magnitude of these effects may depend on the rate of warming across generations. Recent experiments show coral reef fishes can compensate the metabolic challenges of elevated temperature when warm conditions are maintained across generations. However, the effects of a gradual temperature increase across generations remain unknown. In the present study, we analyzed metabolic and molecular traits in the damselfish Acanthochromis polyacanthus that were exposed to +1.5˚C in the first generation and +3.0˚C in the second (Step +3.0˚C). This treatment of step-wise warming was compared to fish reared at current-day temperatures (Control), secondgeneration fish of control parents reared at +3.0˚C (Developmental +3.0˚C), and fish exposed to elevated temperatures for two generations (Transgenerational +1.5˚C and Transgenerational +3.0˚C). Hepatosomatic index, oxygen consumption and liver gene expression were compared in second-generation fish of the multiple treatments. Hepatosomatic index increased in fish that developed at +3.0˚C, regardless of the parental temperature. Routine oxygen consumption of Step +3.0˚C fish was significantly higher than Control, however their aerobic scope recovered to the same level as Control fish. Step +3.0˚C fish exhibited significant upregulation of genes related to mitochondrial activity and energy production, which could be associated to their increased metabolic rates. These results indicate that restoration of aerobic scope is possible when fish experience gradual thermal increase across multiple generations, but the metabolic and molecular responses are different from fish reared at the same elevated thermal conditions in successive generations.
Transgenerational plasticity of reproduction depends on rate of warming across generations
Evolutionary Applications, 2016
Predicting the impacts of climate change to biological systems requires an understanding of the ability for species to acclimate to the projected environmental change through phenotypic plasticity. Determining the effects of higher temperatures on individual performance is made more complex by the potential for environmental conditions experienced in previous and current generations to independently affect phenotypic responses to high temperatures. We used a model coral reef fish (Acanthochromis polyacanthus) to investigate the influence of thermal conditions experienced by two generations on reproductive output and the quality of offspring produced by adults. We found that more gradual warming over two generations, +1.5°C in the first generation and then +3.0°C in the second generation, resulted in greater plasticity of reproductive attributes, compared to fish that experienced the same increase in one generation. Reproduction ceased at the projected future summer temperature (31.5°C) when fish experienced +3.0°C for two generations. Additionally, we found that transgenerational plasticity to +1.5°C induced full restoration of thermally affected reproductive and offspring attributes, which was not possible with developmental plasticity alone. Our results suggest that transgenerational effects differ depending on the absolute thermal change and in which life stage the thermal change is experienced.
Molecular processes of transgenerational acclimation to a warming ocean
Nature Climate Change, 2015
Someanimals have the remarkable capacity to acclimate across generations to projected future climate change1–4; however, the underlying molecular processes are unknown. We sequenced and assembled de novo transcriptomes of adult tropical reef fish exposed developmentally or transgenerationally to projected future ocean temperatures and correlated the resulting expression profiles with acclimated metabolic traits from the same fish. We identified 69 contigs representing 53 key genes involved in thermal acclimation of aerobic capacity. Metabolic genes were among the most upregulated transgenerationally, suggesting shifts in energy production for maintaining performance at elevated temperatures. Furthermore, immune- and stress-responsive genes were upregulated transgenerationally, indicating a new complement of genes allowing the second generation of fish to better cope with elevated temperatures. Other dierentially expressed genes were involved with tissue development and transcriptional regulation. Overall, we found a similar suite of dierentially expressed genes among developmental and transgenerational treatments. Heat-shock protein genes were surprisingly unresponsive, indicating that short-term heat-stress responses may not be a good indicator of long-term acclimation capacity. Our results are the first to reveal the molecular processes that may enable marine fishes to adjust to a future warmer environment over multiple generations.
Adapt, move or die - how will tropical coral reef fishes cope with ocean warming?
Global Change Biology, 2016
Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade more than 365 tropical stenothermal fish species have been documented moving pole-ward, away from ocean warming hotspots where temperatures 2-3 °C above long-term annual means can compromise critical physiological processes. We examined the capacity of a model species-a thermally-sensitive coral reef fish, Chromis viridis (Pomacentridae)to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least six weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope, and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end-of-century predicted temperatures (i.e., 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long-term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating poleward migration of species.
Thermal sensitivity does not determine acclimation capacity for a tropical reef fish
Journal of Animal Ecology, 2012
1. Short-term measures of metabolic responses to warmer environments are expected to indicate the sensitivity of species to regional warming. However, given time, species may be able to acclimate to increasing temperature. Thus, it is useful to determine if short-term responses provide a good predictor for long-term acclimation ability. 2. The tropical reef fish Acanthochromis polyacanthus was used to test whether the ability for developmental thermal acclimation of two populations was indicated by their short-term metabolic response to temperature. 3. While both populations exhibited similar short-term responses of resting metabolic rate (RMR) to temperature, fish from the higher-latitude population were able to fully acclimate RMR, while the lower-latitude population could only partially compensate RMR at the warmest temperature. These differences in acclimation ability are most likely due to genetic differences between the populations rather than differences in thermal regimes. 4. This research indicates that acclimation ability may vary greatly between populations and that understanding such variation will be critical for predicting the impacts of warming environmental temperatures. Moreover, the thermal metabolic reaction norm does not appear to be a good predictor of long-term acclimation ability.
Functional Ecology, 2014
1. Our study addresses the role of non-genetic and genetic inheritance in shaping the adaptive potential of populations under a warming ocean scenario. We used a combined experimental approach [transgenerational plasticity (TGP) and quantitative genetics] to partition the relative contribution of maternal vs. paternal (additive genetic) effects to offspring body size (a key component of fitness), and investigated a potential physiological mechanism (mitochondrial respiration capacities) underlying whole-organism growth/size responses. 2. In very early stages of growth (up to 30 days), offspring body size of marine sticklebacks benefited from maternal TGP: offspring of mothers acclimated to 17°C were larger when reared at 17°C, and offspring of mothers acclimated to 21°C were larger when reared at 21°C. The benefits of maternal TGP on body size were stronger and persisted longer (up to 60 days) for offspring reared in the warmer (21°C) environment, suggesting that maternal effects will be highly relevant for climate change scenarios in this system. 3. Mitochondrial respiration capacities measured on mature offspring (F1 adults) matched the pattern of TGP for juvenile body size, providing an intuitive mechanistic basis for the maternal acclimation persisting into adulthood. Size differences between temperatures seen at early growth stages remained in the F1 adults, linking offspring body size to maternal inheritance of mitochondria. 4. Lower maternal variance components in the warmer environment were mostly driven by mothers acclimated to ambient (colder) conditions, further supporting our tenet that maternal effects were stronger at elevated temperature. Importantly, all parent-offspring temperature combination groups showed genotype 9 environment (G 9 E) interactions, suggesting that reaction norms have the potential to evolve. 5. To summarize, TGP and G 9 E interactions work in concert to mediate impacts of ocean warming on metabolic capacity and early growth of marine sticklebacks. TGP can buffer short-term detrimental effects of climate warming and may buy time for genetic adaptation to catch up, therefore markedly contributing to the evolutionary potential and persistence of populations under climate change.
Ontogeny influences sensitivity to climate change stressors in an endangered fish
Conservation Physiology, 2014
Coastal ecosystems are among the most human-impacted habitats globally, and their management is often critically linked to recovery of declining native species. In the San Francisco Estuary, the Delta Smelt (Hypomesus transpacificus) is an endemic, endangered fish strongly tied to Californian conservation planning. The complex life history of Delta Smelt combined with dynamic seasonal and spatial abiotic conditions result in dissimilar environments experienced among ontogenetic stages, which may yield stage-specific susceptibility to abiotic stressors. Climate change is forecasted to increase San Francisco Estuary water temperature and salinity; therefore, understanding the influences of ontogeny and phenotypic plasticity on tolerance to these critical environmental parameters is particularly important for Delta Smelt and other San Francisco Estuary fishes. We assessed thermal and salinity limits in several ontogenetic stages and acclimation states of Delta Smelt, and paired these data with environmental data to evaluate sensitivity to climate-change stressors. Thermal tolerance decreased among successive stages, with larval fish exhibiting the highest tolerance and post-spawning adults having the lowest. Delta Smelt had limited capacity to increase tolerance through thermal acclimation, and comparisons with field temperature data revealed that juvenile tolerance limits are the closest to current environmental conditions, which may make this stage especially susceptible to future climate warming. Maximal water temperatures observed in situ exceeded tolerance limits of juveniles and adults. Although these temperature events are currently rare, if they increase in frequency as predicted, it could result in habitat loss at these locations despite other favourable conditions for Delta Smelt. In contrast, Delta Smelt tolerated salinities spanning the range of expected environmental conditions for each ontogenetic stage, but salinity did impact survival in juvenile and adult stages in exposures over acute time scales. Our results underscore the importance of considering ontogeny and phenotypic plasticity in assessing the impacts of climate change, particularly for species adapted to spatially and temporally heterogeneous environments. Cite as: Komoroske LM, Connon RE, Lindberg J, Cheng BS, Castillo G, Hasenbein M, Fangue NA (2014) Ontogeny influences sensitivity to climate change stressors in an endangered fish. Conserv Physiol 2: doi:10.1093/conphys/cou008. by guest on March 12, 2014 http://conphys.oxfordjournals.org/ Downloaded from Research article Conservation Physiology • Volume 2 2014 3 Figure 1: Map of the San Francisco Estuary depicting estimated habitat regions for different ontogenetic stages of Delta Smelt, where abiotic conditions, including salinity and temperature, fluctuate spatially and temporally. by guest on March 12, 2014 Figure 2: Thermal tolerance of Delta Smelt. (a) Estimates of chronic lethal thermal maximum (CLT max ; continuous lines) and 95% confidence intervals (dashed lines) for juvenile (blue), adult (red) and post-spawning Delta Smelt (black). Points denote the CLT max50 and CLT max95 estimated mean and 95% confidence interval for each ontogenetic stage on the respective curves. (b) Critical thermal maximum (CT max ) temperatures (means ± SEM) for ontogenetic stages of Delta Smelt at different acclimation temperatures, with jitter (0.05) added to each point to avoid overlapping. Capital letters denote significantly different groups across all ontogenetic stages at medium acclimation temperature only; lower case letters denote significantly different groups among stages of non-larval fish at low, medium and high acclimation temperatures. Within each case, groups not sharing a common letter are significantly different at an adjusted α level of 0.05 as determined by a linear model and pairwise comparisons. PS-Adult denotes post-spawning Delta Smelt. by guest on March 12, 2014 http://conphys.oxfordjournals.org/ Downloaded from Research article Conservation Physiology • Volume 2 2014 The CT max analyses used linear models (Gaussian error distributions), and CLT analysis employed a generalized linear mixed model (binomial error distribution). See text for pairwise comparisons. by guest on March 12, 2014 http://conphys.oxfordjournals.org/ Downloaded from Figure 4: Cumulative proportional survival of juvenile and adult Delta Smelt in acute salinity maximum over 2 weeks of exposure (low salinity, 2.3 ppt, medium salinity, 18.5 ppt; and high salinity, 34.0 ppt). Late-larval data are not shown because they did not exhibit any significant difference in survival across salinity treatments. by guest on March 12, 2014 http://conphys.oxfordjournals.org/ Downloaded from
2016
Transgenerational effects can buffer populations against environmental change, yet little is known about underlying mechanisms, their persistence or the influence of environmental cue timing. We investigated mitochondrial respiratory capacity (MRC) and gene expression of marine sticklebacks that experienced acute or developmental acclimation to simulated ocean warming (21°C) across three generations. Previous work showed that acute acclimation of grandmothers to 21°C led to lower (optimized) offspring MRCs. Here, developmental acclimation of mothers to 21°C led to higher, but more efficient offspring MRCs. Offspring with a 21°C 9 17°C grandmother-mother environment mismatch showed metabolic compensation: their MRCs were as low as offspring with a 17°C thermal history across generations. Transcriptional analyses showed primarily maternal but also grandmaternal environment effects: genes involved in metabolism and mitochondrial protein biosynthesis were differentially expressed when mothers developed at 21°C, whereas 21°C grandmothers influenced genes involved in hemostasis and apoptosis. Genes involved in mitochondrial respiration all showed higher expression when mothers developed at 21°a nd lower expression in the 21°C 9 17°C group, matching the phenotypic pattern for MRCs. Our study links transcriptomics to physiology under climate change, and demonstrates that mechanisms underlying transgenerational effects persist across multiple generations with specific outcomes depending on acclimation type and environmental mismatch between generations.