ALBERT

Description: 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.

Description: 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.

Description: Organisms experience environments that vary across both space and time. Such environmental heterogeneity shapes standing genetic variation and may influence species’ capacity to adapt to rapid environmental change. However, we know little about the kindof genetic variation that is involved in local adaptation to environmental variability. To address this gap, we sequenced the whole genomes of 140 purple sea urchins (Strongylocentrotus purpuratus) from seven populations that vary in their degree of pH variability. Despite no evidence of global population structure, we found a suite of single-nucleotide polymorphisms (SNPs) tightly correlated with local pH variability (outlier SNPs), which were overrepresented in regions putatively involved in gene regulation (long noncoding RNA and enhancers), supporting the idea that variation in regulatory regions is important for local adaptation to variability. In addition, outliers in genes were found to be (i) enriched for biomineralization and ion homeostasis functions related to low pH response, (ii) less central to the protein-protein interaction network, and (iii) underrepresented among genes highly expressed during early development. Taken together, these results suggest that loci that underlie local adaptation to pH variability in purple sea urchins fall in regions with potentially low pleiotropic effects (based on analyses involving regulatory regions, network centrality, and expression time) involved in low pH response (based on functional enrichment).

Description: Significance Resilience to global change will require adaptation to multiple concurrent environmental changes. However, it is unclear if adaptations to multiple stressors can be predicted from the sum of single-stressor adaptation. To answer this question, we experimentally evolved a marine copepod to warming, acidification, and their combination, finding that copepods were able to adapt to all conditions over 25 generations. Warming was a much stronger selective pressure than acidification alone and under multiple-stressor conditions. Nevertheless, the multiple-stressor response to selection was synergistic and unique from either single stressor. Thus, adaptation to single stressors may not reveal adaptive potential or mechanisms of adaptation under multiple stressors, demonstrating the complexity of predicting adaptive responses under multifaceted environmental change. Abstract 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.

Description: Standing genetic variation is important for population persistence in extreme environmental conditions. While some species may have the capacity to adapt to predicted average future global change conditions, the ability to survive extreme events is largely unknown. We used single-generation selection experiments on hundreds of thousands of Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low-pH conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in allele frequencies across replicate cultures for each pH condition and observed increased linkage disequilibrium around selected loci, revealing selection on recombined standing genetic variation. We found that loci responding uniquely to either selection regime were at low starting allele frequencies while variants that responded to both pH conditions (11.6% of selected variants) started at high frequencies. Loci under selection performed functions related to energetics, pH tolerance, cell growth and actin/cytoskeleton dynamics. These results highlight that persistence in future conditions will require two classes of genetic variation: common, pH-responsive variants maintained by balancing selection in a heterogeneous environment, and rare variants, particularly for extreme conditions, that must be maintained by large population sizes.

Description: 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.

Description: Predicting the response of marine animals to climate change is hampered by a lack of multigenerational studies on evolutionary adaptation, particularly to combined ocean warming and acidification (OWA). We provide evidence for rapid adaptation to OWA in the foundational copepod species, Acartia tonsa, by assessing changes in population fitness on the basis of a comprehensive suite of life-history traits, using an orthogonal experimental design of nominal temperature (18 °C, 22 °C) and pCO2 (400, 2,000 µatm) for 25 generations (1 year). Egg production and hatching success initially decreased under OWA, resulting in a 56% reduction in fitness. However, both traits recovered by the third generation, and average fitness was reduced thereafter by only 9%. Antagonistic interactions between warming and acidification in later generations decreased survival, thereby limiting full fitness recovery. Our results suggest that such interactions constrain evolutionary rescue and add complexity to predictions of the responses of animal populations to climate change.