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Differential vulnerability to heatwaves may affect community dynamics in a changing climate. In temperate regions, this vulnerability to heatwaves depends on the interactions between seasonal temperature fluctuations and the capacity to rapidly shift thermal performance curves. Here we investigate how these dynamics affect the vulnerability of two ecologically important copepod congeners,Acartia tonsa, A. hudsonica, to heatwaves of different durations. Using a combination of field observations and simulated laboratory heatwave experiments, we uncover strong seasonal variation in the performance curves of A. tonsa but not A. hudsonica. This translated to species‐specific seasonal patterns of vulnerability to heatwaves, with increased vulnerability in A. hudsonica. By reducing parental stress during simulated heatwaves, seasonal performance curve shifts likely reduced indirect, transgenerational effects of these events on offspring performance in A. tonsa. Our results illustrate how different levels of seasonal variation in thermal performance curves will affect population persistence in a changing climate. 

ABSTRACT The existence of sex‐specific differences in phenotypic traits is widely recognized. Yet they are often ignored in studies looking at the impact of global changes on marine organisms, particularly within the context of combined drivers that are known to elicit complex interactions. We tested sex‐specific physiological responses of the cosmopolitan and ecologically important marine copepodAcartia tonsaexposed to combined hypoxia and marine heatwave (MHW) conditions, both of which individually strongly affect marine ectotherms. Females and males were acutely exposed for 5 days to a combination of either control (18°C) or a high temperature mimicking a MHW (25°C), and normoxia (100% O₂sat.) or mild hypoxia (35% O₂sat.). Life‐history traits, as well as sex‐specific survival and physiological traits, were measured. Females had overall higher thermal tolerance levels and responded differently than males when exposed to the combined global change drivers investigated. Females also showed lower metabolic thermal sensitivity when compared to males. Additionally, the MHW exerted a dominant effect on the traits investigated, causing a lower survival and higher metabolic rate at 25°C. However, egg production rates appeared unaffected by hypoxia and MHW conditions. Our results showed that MHWs could strongly affect copepods' survival, that combined exposure to hypoxia and MHW exerted an interactive effect only on CT_max, and that sex‐specific vulnerability to these global change drivers could have major implications for population dynamics. Our results highlight the importance of considering the differences in the responses of females and males to rapid environmental changes to improve the implementation of climate‐smart conservation approaches. 

Short-term, acute warming events are increasing in frequency across the world’s oceans. For short-lived species like most copepods, these extreme events can occur over both within- and between-generational time scales. Yet, it is unclear whether exposure to acute warming during early life stages of copepods can cause lingering effects on metabolism through development, even after the event has ended. These lingering effects would reduce the amount of energy devoted to growth and affect copepod population dynamics. We exposed nauplii of an ecologically important coastal species, Acartia tonsa , to a 24-hour warming event (control: 18°C; treatment: 28°C), and then tracked individual respiration rate, body length, and stage duration through development. As expected, we observed a decrease in mass-specific respiration rates as individuals developed. However, exposure to acute warming had no effect on the ontogenetic patterns in per-capita or mass-specific respiration rates, body length, or development time. The lack of these carryover effects through ontogeny suggests within-generational resilience to acute warming in this copepod species. 

Phenotypic plasticity and evolutionary adaptation allow populations to cope with global change, but limits and costs to adaptation under multiple stressors are insufficiently understood. We reared a foundational copepod species,Acartia hudsonica, under ambient (AM), ocean warming (OW), ocean acidification (OA), and combined ocean warming and acidification (OWA) conditions for 11 generations (approx. 1 year) and measured population fitness (net reproductive rate) derived from six life-history traits (egg production, hatching success, survival, development time, body size and sex ratio). Copepods under OW and OWA exhibited an initial approximately 40% fitness decline relative to AM, but fully recovered within four generations, consistent with an adaptive response and demonstrating synergy between stressors. At generation 11, however, fitness was approximately 24% lower for OWA compared with the AM lineage, consistent with the cost of producing OWA-adapted phenotypes. Fitness of the OWA lineage was not affected by reversal to AM or low food environments, indicating sustained phenotypic plasticity. These results mimic those of a congener,Acartia tonsa, while additionally suggesting that synergistic effects of simultaneous stressors exert costs that limit fitness recovery but can sustain plasticity. Thus, even when closely related species experience similar stressors, species-specific costs shape their unique adaptive responses. 

Metazoan adaptation to global change relies on selection of standing genetic variation. Determining the extent to which this variation exists in natural populations, particularly for responses to simultaneous stressors, is essential to make accurate predictions for persistence in future conditions. Here, we identified the genetic variation enabling the copepod Acartia tonsa to adapt to experimental ocean warming, acidification, and combined ocean warming and acidification (OWA) over 25 generations of continual selection. Replicate populations showed a consistent polygenic response to each condition, targeting an array of adaptive mechanisms including cellular homeostasis, development, and stress response. We used a genome-wide covariance approach to partition the allelic changes into three categories: selection, drift and replicate-specific selection, and laboratory adaptation responses. The majority of allele frequency change in warming (57%) and OWA (63%) was driven by shared selection pressures across replicates, but this effect was weaker under acidification alone (20%). OWA and warming shared 37% of their response to selection but OWA and acidification shared just 1%, indicating that warming is the dominant driver of selection in OWA. Despite the dominance of warming, the interaction with acidification was still critical as the OWA selection response was highly synergistic with 47% of the allelic selection response unique from either individual treatment. These results disentangle how genomic targets of selection differ between single and multiple stressors and demonstrate the complexity that nonadditive multiple stressors will contribute to predictions of adaptation to complex environmental shifts caused by global change. 

Abstract Copepods are key components of aquatic habitats across the globe. Understanding how they respond to warming is important for predicting the effects of climate change on aquatic communities. Lethal thermal limits may play an important role in determining responses to warming. Thermal tolerance can vary over several different spatial and temporal scales, but we still lack a fundamental understanding of what drives the evolution of these patterns in copepods. In this Horizons piece, we provide a synthesis of global patterns in copepod thermal tolerance and potential acclimatory capacities. Copepod thermal tolerance increases with maximum annual temperature. We also find that the effects of phenotypic plasticity on thermal tolerance are negatively related to the magnitude of thermal tolerance, suggesting a potential trade-off between these traits. Our ability to fully describe these patterns is limited, however, by a lack of spatial, temporal and phylogenetic coverage in copepod thermal tolerance data. We indicate several priority areas for future work on copepod thermal tolerance, and accompanying suggestions regarding experimental design and methodology. 

Organisms experience variation in the thermal environment on several different temporal scales, with seasonality being particularly prominent in temperate regions. For organisms with short generation times, seasonal variation is experienced across, rather than within, generations. How this affects the seasonal evolution of thermal tolerance and phenotypic plasticity is understudied, but has direct implications for the thermal ecology of these organisms. Here we document intra-annual patterns of thermal tolerance in two species of Acartia copepods (Crustacea) from a highly seasonal estuary, showing strong variation across the annual temperature cycle. Common garden, split-brood experiments indicate that this seasonal variation in thermal tolerance, along with seasonal variation in body size and phenotypic plasticity, is likely affected by genetic polymorphism. Our results show that adaptation to seasonal variation is important to consider when predicting how populations may respond to ongoing climate change.