Genetic differentiation underlies seasonal variation in thermal tolerance, body size, and plasticity in a short‐lived copepod

Sasaki, Matthew; Dam, Hans G.

doi:10.1002/ece3.6851

Cited by 32 publications

(43 citation statements)

References 105 publications

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“…Populations sampled along a latitudinal gradient show a trade-off between thermal tolerance and degree of developmental plasticity 66 . The same pattern is observed in A. tonsa populations throughout the season 67 .…”

Section: Resultssupporting

confidence: 79%

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

Brennan

deMayo

Dam

et al. 2020

Preprint

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Global conditions are changing at unprecedented rates (1), challenging species resilience (2). Populations can respond to these changes through genetic adaptation and physiological plasticity (3, 4), and it is well accepted that these processes interact (5). However, the relative role plasticity and adaptation play in promoting resilience to global change and the potential impacts of rapid adaptation on plasticity during this process are not well understood (3, 5–10). Here, using experimental evolution and reciprocal transplantation of the marine coastal copepod, Acartia tonsa, we show rapid adaptation to global change conditions carries costs, notably a loss of physiological plasticity. Twenty generations of selection resulted in rapid, highly parallel adaptation to greenhouse conditions. However, this adaptation reduced plasticity and fitness, particularly when returned to ambient conditions and under food limitation. Due to the loss of plasticity, greenhouse adapted lines could no longer tolerate ambient conditions and compensated by additional adaptive evolution, a process that eroded nucleotide diversity in genes containing adaptive genetic variation for global change conditions. These results show that adaptation can negatively affect plasticity, limiting resilience to new stressors and previously benign environments. Our findings challenge the common assertion that the presence of adaptive genetic potential or physiological plasticity alone will enable population resilience under global change conditions.Significance statementUnderstanding how species will respond to changing environmental conditions is an essential step in mitigating the potential negative consequences of human induced global change conditions. Typically, it is assumed that a species with sufficient plasticity or adaptive potential will be resilient in the face of these changes. Here, we experimentally evolve a copepod to simulated future acidic and warm conditions. We show that rapid adaptation reduced phenotypic plasticity and eroded the adaptive genetic variation necessary to tolerate additional environmental stress. These findings demonstrate that the presence of plasticity or adaptive potential do not necessarily indicate a resilient population, illustrating the importance of considering the interaction between these factors when predicting species tolerance to global change.

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Section: Resultssupporting

confidence: 79%

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

Brennan

deMayo

Dam

et al. 2020

Preprint

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“…After accounting for the observed changes in the Control lineages, there was still a significant negative correlation between changes in thermal tolerance and changes in tolerance plasticity. Interestingly, this negative relationship has also been observed in patterns of the evolution of plasticity in thermal tolerance for copepods over large spatial scales and across the seasonal temperature cycle (Sasaki & Dam, 2019 , 2020 ), suggesting that this trade‐off may be a widespread phenomenon in planktonic copepods. However, it should be noted that there are several other potential mechanisms besides a true mechanistic trade‐off that might result in a negative relationship between tolerance and tolerance plasticity (van Heerwaarden & Kellermann, 2020 ).…”

Section: Discussionmentioning

confidence: 87%

“…The rapid rate of change we observed is in agreement with the generally rapid responses to selection observed in this and other copepod taxa (Kelly, DeBiasse et al, 2016 ; Langer et al, 2019 ; Lee et al, 2011 ; Colin & Dam, 2005 ). Previous work with Acartia tonsa found evidence for local adaptation of thermal tolerance over various spatial scales (González, 1974 ; Sasaki & Dam, 2019 ; Sasaki et al, 2019 ) and over relatively short seasonal timescales (Sasaki & Dam, 2020 ). Further, this species is characterized by high levels of cryptic genetic diversity (Caudill & Bucklin, 2004 ; Chen & Hare, 2011 ; Sasaki & Dam, 2019 ).…”

Section: Discussionmentioning

confidence: 96%

“…Further, because of these copepods' relatively short generation times (usually <1 month), these seasonal temperature cycles are experienced across generations, rather than within. This cyclical temperature variation may maintain adaptive genetic variation in both thermal tolerance and plasticity in thermal tolerance (Sasaki & Dam, 2020 ), priming populations to respond to changes in mean temperature. Rather than the effects of lethal selection on thermal tolerance, our choice of temperatures examines the capacity for standing genetic variation to respond to chronic, sublethal temperature differences.…”

Section: Methodsmentioning

confidence: 99%

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Negative relationship between thermal tolerance and plasticity in tolerance emerges during experimental evolution in a widespread marine invertebrate

Sasaki

Dam

2021

Evolutionary Applications

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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 copepod Acartia 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.

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“…Targeted tests of the evolutionary theory appear to be largely confined to terrestrial systems. It is only within the last year that studies have conducted effective tests of theoretical predictions using marine populations [20,[42][43][44]. The generality of theoretical predictions hinges upon more effectively including the range of systems exposed to patterns of fluctuating selection in empirical research.…”

Section: Empirical Progressmentioning

confidence: 99%

Fluctuating selection and global change: a synthesis and review on disentangling the roles of climate amplitude, predictability and novelty

et al. 2021

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A formidable challenge for global change biologists is to predict how natural populations will respond to the emergence of conditions not observed at present, termed novel climates. Popular approaches to predict population vulnerability are based on the expected degree of novelty relative to the amplitude of historical climate fluctuations experienced by a population. Here, we argue that predictions focused on amplitude may be inaccurate because they ignore the predictability of environmental fluctuations in driving patterns of evolution and responses to climate change. To address this disconnect, we review major findings of evolutionary theory demonstrating the conditions under which phenotypic plasticity is likely to evolve in natural populations, and how plasticity decreases population vulnerability to novel environments. We outline key criteria that experimental studies should aim for to effectively test theoretical predictions, while controlling for the degree of climate novelty. We show that such targeted tests of evolutionary theory are rare, with marine systems being overall underrepresented in this venture despite exhibiting unique opportunities to test theory. We conclude that with more robust experimental designs that manipulate both the amplitude and predictability of fluctuations, while controlling for the degree of novelty, we may better predict population vulnerability to climate change.

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Genetic differentiation underlies seasonal variation in thermal tolerance, body size, and plasticity in a short‐lived copepod

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 32 publications

References 105 publications

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

Negative relationship between thermal tolerance and plasticity in tolerance emerges during experimental evolution in a widespread marine invertebrate

Fluctuating selection and global change: a synthesis and review on disentangling the roles of climate amplitude, predictability and novelty

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