Abstract Under climate change, ectotherms will likely face pressure to adapt to novel thermal environments by increasing their upper thermal tolerance and its plasticity, a measure of thermal acclimation. Ectotherm populations with high thermal tolerance are often less thermally plastic, a trade‐off hypothesized to result from (i) a phenotypic limit on thermal tolerance above which plasticity cannot further increase the trait, (ii) negative genetic correlation or (iii) fitness trade‐offs between the two traits. Whether each hypothesis causes negative associations between thermal tolerance and plasticity has implications for the evolution of each trait.We empirically tested the limit and trade‐off hypotheses by leveraging the experimental tractability and thermal biology of the intertidal copepodTigriopus californicus. Using populations from four latitudinally distributed sites in coastal California, six lines per population were reared under a laboratory common garden for two generations. Ninety‐six full sibling replicates (n = 4–5 per line) from a third generation were developmentally conditioned to 21.5 and 16.5°C until adulthood. We then measured the upper thermal tolerance and fecundity of sibships at each temperature.We detected a significant trade‐off in fecundity, a fitness corollary, between baseline thermal tolerance and its plasticity.Tigriopus californicuspopulations and genotypes with higher thermal tolerance were less thermally plastic. We detected negative directional selection on thermal plasticity under ambient temperature evidenced by reduced fecundity. These fitness costs of plasticity were significantly higher among thermally tolerant genotypes, consistent with the trade‐off hypothesis. This trade‐off was evident under ambient conditions, but not high temperature.Observed thermal plasticity and fecundity were best explained by a model incorporating both the limit and trade‐off hypotheses rather than models with parameters associated with one hypothesis. Effects of population and family on tolerance and plasticity negatively covaried, suggesting that a negative genetic correlation could not be ruled as contributing to negative associations between the traits. Our study provides a novel empirical test of the fitness trade‐off hypothesis that leverages a strong inference approach. We discuss our results' insights into how thermal adaptation may be constrained by physiological limits, genetic correlations, and fitness trade‐offs between thermal tolerance and its plasticity. Read the freePlain Language Summaryfor this article on the Journal blog.
more »
« less
Evaluating the fitness consequences of plasticity in tolerance to pesticides
Abstract In a rapidly changing world, phenotypic plasticity may be a critical mechanism allowing populations to rapidly acclimate when faced with novel anthropogenic stressors. Theory predicts that if exposure to anthropogenic stress is heterogeneous, plasticity should be maintained as it allows organisms to avoid unnecessary expression of costly traits (i.e., phenotypic costs) when stressors are absent. Conversely, if exposure to stressors becomes constant, costs or limits of plasticity may lead to evolutionary trait canalization (i.e., genetic assimilation). While these concepts are well‐established in theory, few studies have examined whether these factors explain patterns of plasticity in natural populations facing anthropogenic stress. Using wild populations of wood frogs that vary in plasticity in tolerance to pesticides, the goal of this study was to evaluate the environmental conditions under which plasticity is expected to be advantageous or detrimental. We found that when pesticides were absent, more plastic populations exhibited lower pesticide tolerance and were more fit than less plastic populations, likely avoiding the cost of expressing high tolerance when it was not necessary. Contrary to our predictions, when pesticides were present, more plastic populations were as fit as less plastic populations, showing no signs of costs or limits of plasticity. Amidst unprecedented global change, understanding the factors shaping the evolution of plasticity will become increasingly important.
more »
« less
- PAR ID:
- 10458182
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 10
- Issue:
- 10
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- p. 4448-4456
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Phenotypic plasticity is the primary mechanism of organismal resilience to abiotic and biotic stress, and genetic differentiation in plasticity can evolve if stresses differ among populations. Inducible defence is a common form of adaptive phenotypic plasticity, and long‐standing theory predicts that its evolution is shaped by costs of the defensive traits, costs of plasticity and a trade‐off in allocation to constitutive versus induced traits. We used a common garden to study the evolution of defence in two native populations of wild arugulaEruca sativa(Brassicaceae) from contrasting desert and Mediterranean habitats that differ in attack by caterpillars and aphids. We report genetic differentiation and additive genetic variance for phenology, growth and three defensive traits (toxic glucosinolates, anti‐nutritive protease inhibitors and physical trichome barriers) as well their inducibility in response to the plant hormone jasmonic acid. The two populations were strongly differentiated for plasticity in nearly all traits. There was little evidence for costs of defence or plasticity, but constitutive and induced traits showed a consistent additive genetic trade‐off within each population for the three defensive traits. We conclude that these populations have evolutionarily diverged in inducible defence and retain ample potential for the future evolution of phenotypic plasticity in defence.more » « less
-
ABSTRACT Evolutionary responses to climate change may incur trade‐offs due to energetic constraints and mechanistic limitations, which are both influenced by environmental context. Adaptation to one stressor may result in life history trade‐offs, canalization of phenotypic plasticity, and the inability to tolerate other stressors, among other potential costs. While trade‐offs incurred during adaptation are difficult to detect in natural populations, experimental evolution can provide important insights by measuring correlated responses to selection as populations adapt to changing environments. However, studies testing for trade‐offs have generally lagged behind the growth in the use of experimental evolution in climate change studies. We argue that the important insights generated by the few studies that have tested for trade‐offs make a strong case for including these types of measurements in future studies of climate adaptation. For example, there is emerging consensus from experimental evolution studies that tolerance and tolerance plasticity trade‐offs are an often‐observed outcome of adaptation to anthropogenic change. In recent years, these types of studies have been strengthened by the use of sequencing of experimental populations, which provides promising new avenues for understanding the molecular mechanisms underlying observed phenotypic trade‐offs.more » « less
-
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.more » « less
-
Local adaptation in a marine foundation species: Implications for resilience to future global changeAbstract Environmental change is multidimensional, with local anthropogenic stressors and global climate change interacting to differentially impact populations throughout a species’ geographic range. Within species, the spatial distribution of phenotypic variation and its causes (i.e., local adaptation or plasticity) will determine species’ adaptive capacity to respond to a changing environment. However, comparatively less is known about the spatial scale of adaptive differentiation among populations and how patterns of local adaptation might drive vulnerability to global change stressors. To test whether fine‐scale (2–12 km) mosaics of environmental stress can cause adaptive differentiation in a marine foundation species, eelgrass (Zostera marina), we conducted a three‐way reciprocal transplant experiment spanning the length of Tomales Bay, CA. Our results revealed strong home‐site advantage in growth and survival for all three populations. In subsequent common garden experiments and feeding assays, we showed that countergradients in temperature, light availability, and grazing pressure from an introduced herbivore contribute to differential performance among populations consistent with local adaptation. Our findings highlight how local‐scale mosaics in environmental stressors can increase phenotypic variation among neighboring populations, potentially increasing species resilience to future global change. More specifically, we identified a range‐center eelgrass population that is pre‐adapted to extremely warm temperatures similar to those experienced by low‐latitude range‐edge populations of eelgrass, demonstrating how reservoirs of heat‐tolerant phenotypes may already exist throughout a species range. Future work on predicting species resilience to global change should incorporate potential buffering effects of local‐scale population differentiation and promote a phenotypic management approach to species conservation.more » « less
An official website of the United States government
