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Biology subjects

Dam, H. G.

Publications and source records attributed to Dam, H. G..

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Epigenetic and evolutionary mechanisms uniquely contribute to rescue from global change

To persist in the geologically unprecedented rates of global change, populations can adapt or acclimate. However, how these mechanisms of resilience interact, particularly the role of epigenetic variation in long-term adaptation, is unknown. To address this gap, we experimentally evolved the foundational marine copepod Acartia tonsa for 25 generations under ocean acidification, warming, their combination, and control conditions then measured epigenomic, genomic, and transcriptomic responses. We observed clear and consistent epigenomic and genomic divergence between treatments, with epigenomic divergence concentrated in genes related to stress response and the regulation of transposable elements. However, epigenetic and genetic changes occurred in different regions of the genome such that regions with significant methylation divergence had 2-2.5 fold lower FST than regions without methylation divergence. This negative relationship between epigenetic and genetic divergence could be driven by local inhibition of one another or distinct functional targets of selection. In contrast, epigenetic divergence was positively linked to gene expression divergence, indicating that epigenetic changes may facilitate phenotypic change. Taken together, these results suggest that unique, complementary genetic and epigenetic mechanisms promote resilience to global change. Significance StatementOrganisms must adapt or acclimate to survive global change, but how these processes interact and the role of epigenetic variation is unknown. To address these gaps, we experimentally evolved the marine copepod Acartia tonsa for 25 generations in global change conditions and measured their genomic, epigenomic, and gene expression responses. We found that both genetic and epigenetic changes contributed to resilience and were inversely related, acting in different regions of the genome. Epigenetic changes were functionally linked to the regulation of stress and transposable elements and correlated with shifts in gene expression. Therefore, the resilience of populations to ongoing global change is driven by the complementary contribution of both genetic and epigenetic mechanisms.

evolutionary biology↗

Seasonally variable thermal performance curves prevent adverse effects of heatwaves

The increasing frequency and intensity of heatwaves may represent a significant challenge for predicting vulnerability of populations in a warming ocean. The direct impacts of heatwaves on populations depend on the relative position of environmental temperatures to the thermal performance curve optima. If thermal performance curves are static, the effects of heatwaves may therefore change seasonally over the annual temperature cycle. However, these seasonal changes in the effects of heatwaves may be dampened by corresponding variation in thermal performance curves which, in organisms with relatively short generation times, may be driven by phenotypic plasticity as well as genetic differentiation. Here we investigate the effects of seasonal timing and duration on the impacts of heatwaves in the ecologically important copepod congeners Acartia tonsa and Acartia hudsonica, and test the hypotheses that 1) seasonal variation in thermal performance curves will reduce overall population vulnerability to heatwaves, and 2) that seasonal variation in TPCs will prevent negative transgenerational effects of heatwave. We characterized seasonal variation in thermal performance curves for several fitness-related traits. These experiments uncovered strong seasonal variation in the thermal performance curves of Acartia tonsa, and indicate that this variation buffers against negative effects of simulated heatwaves. We also quantified both direct and trans-generational effects of different duration heatwaves on copepods collected at various times throughout the season using simulated heatwave experiments. There was no consistent pattern in the transgenerational effects of parental exposure to heatwaves, which may indicate that seasonal variation in thermal performance curves reduces the effects of parental stress on offspring performance. Our results show that seasonal variation in thermal performance curves will likely play an important role in limiting the adverse effects of heatwaves on populations.

ecology↗

Parasitism does not reduce thermal limits in the intermediate host of a bopyrid isopod

Parasitism has strong effects on community dynamics. Given the detrimental effects parasites have on host health, infection or infestation might be expected to reduce upper thermal limits, increasing the vulnerability of host species to future climate change. Copepods are integral components of aquatic food webs and biogeochemical cycles. They also serve as intermediate hosts in the life cycle of parasitic isopods in the family Bopyridae. Given the important effects both copepods and isopod parasites play in aquatic communities, it is important to understand how the interaction between parasite and host affects thermal limits in order to better predict how community dynamics may change in a warming climate. Here we examined the effect of infestation by larvae of a bopyrid isopod on cosmopolitan copepod Acartia tonsa to test the hypothesis that infestation reduces thermal limits. To aid with this work, we developed an affordable, highly portable system for measuring critical thermal maxima of small ectotherms. We also used meta-analysis to summarize the effects of parasitism on critical thermal maxima in a wider range of taxa to help contextualize our findings. Contrary to both our hypothesis and the results of previous studies, we observed no reduction of thermal limits by parasitism in A. tonsa. These results suggest that life history of the host and parasite may interact to determine how parasite infestation affects environmental sensitivity.

physiology↗

Naupliar exposure to acute warming does not affect ontogenetic patterns in respiration, body size, or development time in the cosmopolitan copepod Acartia tonsa

Short-term, acute warming events are increasing in frequency across the worlds 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{degrees}C; treatment: 28{degrees}C), and then tracked individual respiration rate, body length, and stage duration through development. As expected, we observed a decrease in massspecific 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.

physiology↗

Experimental evolution reveals the synergistic genomic mechanisms of adaptation to ocean warming and acidification in a marine copepod

Metazoan adaptation to global change will rely on selection of standing genetic variation. Determining the extent to which this variation exists in natural populations, particularly for responses to simultaneous stressors, is therefore essential to make accurate predictions for persistence in future conditions. Here, we identify the genetic variation enabling the copepod Acartia tonsa to adapt to experimental ocean warming, acidification, and combined ocean warming and acidification (OWA) conditions over 25 generations. Replicate populations showed a strong and 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 genomic changes into selection, drift, and lab adaptation and found that the majority of allele frequency change in warming (56%) and OWA (63%) was driven by selection but acidification was dominated by drift (66%). OWA and warming shared 37% of their response to selection but OWA and acidification shared just 1%. Accounting for lab adaptation was essential for not inflating a shared response to selection between all treatments. Finally, the mechanisms of adaptation in the multiple-stressor OWA conditions were not an additive product of warming and acidification, but rather a synergistic response where 47% of the allelic responses to selection were unique. These results are among the first to disentangle how the genomic targets of selection differ between single and multiple stressors and to demonstrate the complexity that non-additive multiple stressors will contribute to attempts to predict adaptive responses to complex environments.

evolutionary biology↗

Rapid, but limited, zooplankton adaptation to simultaneous warming and acidification

Predicting the response of marine metazoans to climate change is hampered by a lack of 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 based on a comprehensive suite of life-history traits, using an orthogonal experimental design of nominal temperature (18{degrees}C, 22{degrees}C) and pCO2 (400, 2000 atm) 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 such interactions constrain evolutionary rescue and add complexity to predictions of the responses of metazoan populations to climate change.

evolutionary biology↗

Global change adaptation limits future resilience

Adaptive evolution from standing genetic variation and physiological plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earths oceans. For marine animals, however, we have much to learn about the mechanisms, interactions, and costs of adaptation. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplantation, we investigate the relationship between adaptation and plasticity in the marine copepod, Acartia tonsa, in future greenhouse conditions (high temperature, high CO2). We find highly parallel genetic adaptation to greenhouse conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that genetic adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when greenhouse animals were returned to ambient conditions or reared in low food conditions, suggestive of genetic assimilation after 20 generations of adaptation. Despite the loss of plasticity at F21, after three successive transplant generations, greenhouse-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 the power of experimental evolution from natural populations to reveal the mechanisms, timescales of responses, consequences, and reversibility of complex, physiological adaptation. While plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations genetically adapted, limiting resilience to new stressors and previously benign environments.

evolutionary biology↗

Complex interactions between local adaptation, plasticity, and sex affect vulnerability to warming in a widespread marine copepod

Predicting the response of populations to climate change requires knowledge of thermal performance. Genetic differentiation and phenotypic plasticity affect thermal performance, but the effects of sex and developmental temperatures often go uncharacterized. We used common garden experiments to test for effects of local adaptation, developmental phenotypic plasticity, and individual sex on thermal performance of the ubiquitous copepod, Acartia tonsa. Females had higher thermal tolerance than males in both populations, while the Florida population had higher thermal tolerance compared to the Connecticut population. An effect of developmental phenotypic plasticity on thermal tolerance was observed only in the Connecticut population. Ignoring sex-specific differences may result in a severe underestimation of population-level impacts of warming (i.e. - population decline due to sperm limitation). Further, despite having a higher thermal tolerance, southern populations may be more vulnerable to warming as they lack the ability to respond to increases in temperature through phenotypic plasticity.

evolutionary biology↗