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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. 

Climate change is resulting in increasing ocean temperatures and salinity variability, particularly in estuarine environments. Tolerance of temperature and salinity change interact and thus may impact organismal resilience. Populations can respond to multiple stressors in the short‐term (i.e., plasticity) or over longer timescales (i.e., adaptation). However, little is known about the short‐ or long‐term effects of elevated temperature on the tolerance of acute temperature and salinity changes. Here, we characterized the response of the near‐shore and estuarine copepod,Acartia tonsa, to temperature and salinity stress. Copepods originated from one of two sets of replicated >40 generation‐old temperature‐adapted lines: ambient (AM, 18°C) and ocean warming (OW, 22°C). Copepods from these lines were subjected to one and three generations at the reciprocal temperature. Copepods from all treatments were then assessed for differences in acute temperature and salinity tolerance. Development (one generation), three generations, and >40 generations of warming increased thermal tolerance compared to Ambient conditions, with development in OW resulting in equal thermal tolerance to three and >40 generations of OW. Strikingly, developmental OW and >40 generations of OW had no effect on low salinity tolerance relative to ambient. By contrast, when environmental salinity was reduced first, copepods had lower thermal tolerances. These results highlight the critical role for plasticity in the copepod climate response and suggest that salinity variability may reduce copepod tolerance to subsequent warming.

 

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. 

Adaptive evolution and phenotypic plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earth’s oceans, however, we have much to learn about the interactions and costs of these mechanisms of resilience. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplants, we investigated the relationship between adaptation and plasticity in the marine copepod,Acartia tonsa, in future global change conditions (high temperature and high CO₂). We found parallel adaptation to global change conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when global change-adapted animals were returned to ambient conditions or reared in low food conditions. However, after three successive transplant generations, global change-adapted animals were able to match the ambient-adaptive transcriptional profile. Concurrent changes in allele frequencies and erosion of nucleotide diversity suggest that this recovery occurred via adaptation back to ancestral conditions. These results demonstrate that while plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations adapted, limiting resilience to new stressors and previously benign environments.

 

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. 

Whether populations can adapt to predicted climate change conditions, and how rapidly, are critical questions for the management of natural systems. Experimental evolution has become an important tool to answer these questions. In order to provide useful, realistic insights into the adaptive response of populations to climate change, there needs to be careful consideration of how genetic differentiation and phenotypic plasticity interact to generate observed phenotypic changes. We exposed three populations of the widespread copepodAcartia tonsa(Crustacea) to chronic, sublethal temperature selection for 15 generations. We generated thermal survivorship curves at regular intervals both during and after this period of selection to track the evolution of thermal tolerance. Using reciprocal transplants between ambient and warming conditions, we also tracked changes in the strength of phenotypic plasticity in thermal tolerance. We observed significant increases in thermal tolerance in the Warming lineages, while plasticity in thermal tolerance was strongly reduced. We suggest these changes are driven by a negative relationship between thermal tolerance and plasticity in thermal tolerance. Our results indicate that adaptation to warming through an increase in thermal tolerance might not reduce vulnerability to climate change if the increase comes at the expense of tolerance plasticity. These results illustrate the importance of considering changes in both a trait of interest and the trait plasticity during experimental evolution.

 

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 ofAcartiacopepods (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.