ALBERT

Description: Increasing climate variability may pose an even greater risk to species than climate warming because temperature fluctuations can amplify adverse impacts of directional warming on fitness-related traits. Here, the influence of directional warming and increasing climate variability on marine stickleback fish (Gasterosteus aculeatus) offspring size variation was investigated by simulating changes to the mean and variance of ocean temperatures predicted under climate change. Reproductive traits of mothers and offspring size reaction norms across four climate scenarios were examined to assess the roles of standing genetic variation, transgenerational and within-generation plasticity in adaptive potential. Mothers acclimated to directional warming produced smaller eggs than mothers in constant, ambient temperatures, whereas mothers in a predictably variable environment (weekly change between temperatures) produced a range of egg sizes, possibly reflecting a diversified bet hedging strategy. Offspring size post-hatch was mostly influenced by genotype by environment interactions and not transgenerational effects. Offspring size reaction norms also differed depending on the type of environmental predictability (predictably variable vs. stochastic), with offspring reaching the largest sizes in the stochastic environment. Release of cryptic genetic variation for offspring size in the stochastic environment suggests hidden evolutionary potential in this wild population to respond to changes in environmental predictability.

Description: Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within-clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17 °C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21 °C), implying selection for different-sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within-female egg size variability, especially at 21 °C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21 °C had larger mean body sizes if their mother developed at 21 °C, but this TGP benefit was not present for offspring of 17 °C mothers reared at 17 °C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21 °C. In summary, stickleback mothers may have used both TGP and diversified bet-hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty.

Description: Nongenetic inheritance mechanisms such as transgenerational plasticity (TGP) can buffer populations against rapid environmental change such as ocean warming. Yet, little is known about how long these effects persist and whether they are cumulative over generations. Here, we tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks. Grandparents were acclimated for two months during reproductive conditioning, whereas parents experienced developmental acclimation, allowing us to compare the fitness consequences of short-term vs. prolonged exposure to elevated temperature across multiple generations. We found that reproductive output of F1 adults was primarily determined by maternal developmental temperature, but carry-over effects from grandparental acclimation environments resulted in cumulative negative effects of elevated temperature on hatching success. In very early stages of growth, F2 offspring reached larger sizes in their respective paternal and grandparental environment down the paternal line, suggesting that other factors than just the paternal genome may be transferred between generations. In later growth stages, maternal and maternal granddam environments strongly influenced offspring body size, but in opposing directions, indicating that the mechanism(s) underlying the transfer of environmental information may have differed between acute and developmental acclimation experienced by the two generations. Taken together, our results suggest that the fitness consequences of parental and grandparental TGP are highly context dependent, but will play an important role in mediating some of the impacts of rapid climate change in this system.

Description: Background: Pathogens are a major regulatory force for host populations, especially under stressful conditions. Elevated temperatures may enhance the development of pathogens, increase the number of transmission stages, and can negatively influence host susceptibility depending on host thermal tolerance. As a net result, this can lead to a higher prevalence of epidemics during summer months. These conditions also apply to marine ecosystems, where possible ecological impacts and the population-specific potential for evolutionary responses to changing environments and increasing disease prevalence are, however, less known. Therefore, we investigated the influence of thermal stress on the evolutionary trajectories of disease resistance in three marine populations of three-spined sticklebacks Gasterosteus aculeatus by combining the effects of elevated temperature and infection with a bacterial strain of Vibrio sp. using a common garden experiment. Results: We found that thermal stress had an impact on fish weight and especially on survival after infection after only short periods of thermal acclimation. Environmental stress reduced genetic differentiation (QST) between populations by releasing cryptic within-population variation. While life history traits displayed positive genetic correlations across environments with relatively weak genotype by environment interactions (GxE), environmental stress led to negative genetic correlations across environments in pathogen resistance. This reversal of genetic effects governing resistance is probably attributable to changing environment-dependent virulence mechanisms of the pathogen interacting differently with host genotypes, i.e. GPathogenxGHostxE or (GPathogenxE)x(GHostxE) interactions, rather than to pure host genetic effects, i.e. GHostxE interactions. Conclusion: To cope with climatic changes and the associated increase in pathogen virulence, host species require wide thermal tolerances and pathogen-resistant genotypes. The higher resistance we found for some families at elevated temperatures showed that there is evolutionary potential for resistance to Vibrio sp. in both thermal environments. The negative genetic correlation of pathogen resistance between thermal environments, on the other hand, indicates that adaptation to current conditions can be a weak predictor for performance in changing environments. The observed feedback on selective gradients exerted on life history traits may exacerbate this effect, as it can also modify the response to selection for other vital components of fitness.

Description: 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 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 transgenerational plasticity (TGP): offspring of mothers acclimated to17°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 x environment (GxE) interactions, suggesting that reaction norms have the potential to evolve. 5) To summarise, transgenerational plasticity and genotype x environment 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.

Description: 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 (optimised) offspring MRCs. Here, developmental acclimation of mothers to 21°C led to higher, but more efficient offspring MRCs. Offspring with a 21°Cx17°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° and lower expression in the 21°Cx17°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.