skip to main content

Title: Genetic differentiation underlies seasonal variation in thermal tolerance, body size, and phenotypic plasticity in a short-lived copepod
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.
Authors:
;
Award ID(s):
1947965
Publication Date:
NSF-PAR ID:
10252712
Journal Name:
Ecology and evolution
Volume:
10
Issue:
21
Page Range or eLocation-ID:
12200-12210
ISSN:
2045-7758
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT Cities are emerging as a new venue to overcome the challenges of obtaining data on compensatory responses to climatic warming through phenotypic plasticity and evolutionary change. In this Review, we highlight how cities can be used to explore physiological trait responses to experimental warming, and also how cities can be used as human-made space-for-time substitutions. We assessed the current literature and found evidence for significant plasticity and evolution in thermal tolerance trait responses to urban heat islands. For those studies that reported both plastic and evolved components of thermal tolerance, we found evidence that both mechanisms contributed to phenotypicmore »shifts in thermal tolerance, rather than plastic responses precluding or limiting evolved responses. Interestingly though, for a broader range of studies, we found that the magnitude of evolved shifts in thermal tolerance was not significantly different from the magnitude of shift in those studies that only reported phenotypic results, which could be a product of evolution, plasticity, or both. Regardless, the magnitude of shifts in urban thermal tolerance phenotypes was comparable to more traditional space-for-time substitutions across latitudinal and altitudinal clines in environmental temperature. We conclude by considering how urban-derived estimates of plasticity and evolution of thermal tolerance traits can be used to improve forecasting methods, including macrophysiological models and species distribution modelling approaches. Finally, we consider areas for further exploration including sub-lethal performance traits and thermal performance curves, assessing the adaptive nature of trait shifts, and taking full advantage of the environmental thermal variation that cities generate.« less
  2. Cooke, Steve (Ed.)
    Abstract Models of species response to climate change often assume that physiological traits are invariant across populations. Neglecting potential intraspecific variation may overlook the possibility that some populations are more resilient or susceptible than others, creating inaccurate predictions of climate impacts. In addition, phenotypic plasticity can contribute to trait variation and may mediate sensitivity to climate. Quantifying such forms of intraspecific variation can improve our understanding of how climate can affect ecologically important species, such as invasive predators. Here, we quantified thermal performance (tolerance, acclimation capacity, developmental traits) across seven populations of the predatory marine snail (Urosalpinx cinerea) from nativemore »Atlantic and non-native Pacific coast populations in the USA. Using common garden experiments, we assessed the effects of source population and developmental acclimation on thermal tolerance and developmental traits of F1 snails. We then estimated climate sensitivity by calculating warming tolerance (thermal tolerance − habitat temperature), using field environmental data. We report that low-latitude populations had greater thermal tolerance than their high latitude counterparts. However, these same low-latitude populations exhibited decreased thermal tolerance when exposed to environmentally realistic higher acclimation temperatures. Low-latitude native populations had the greatest climate sensitivity (habitat temperatures near thermal limits). In contrast, invasive Pacific snails had the lowest climate sensitivity, suggesting that these populations are likely to persist and drive negative impacts on native biodiversity. Developmental rate significantly increased in embryos sourced from populations with greater habitat temperature but had variable effects on clutch size and hatching success. Thus, warming can produce widely divergent responses within the same species, resulting in enhanced impacts in the non-native range and extirpation in the native range. Broadly, our results highlight how intraspecific variation can alter management decisions, as this may clarify whether management efforts should be focused on many or only a few populations.« less
  3. 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 findmore »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.« less
  4. Adaptive thermal plasticity allows organisms to adjust their physiology to cope with fluctuating environments. However, thermal plasticity is rarely studied in response to thermal variability and is often measured in a single life stage. Plasticity in response to thermal variability likely differs from responses to constant temperatures or acute stress. In addition, life stages likely differ in their plasticity and responses in one stage may be affected by the experiences in a previous stage. Increasing the resolution with which we understand thermal plasticity in response to thermal variation across ontogeny is crucial to understanding how organisms cope with the thermalmore »variation in their environment and to estimating the capacity of plasticity to mitigate costs of rapid environmental change. We wanted to know if life stages differ in their capacity for thermal plasticity under temperature fluctuations. We reared Onthophagus taurus dung beetles in either low or high temperature fluctuation treatments and quantified thermal plasticity of metabolism of pupae and adults. We found that adults were thermally plastic and pupae were not. Next, we wanted to know if the plasticity observed in the adult life stage was affected by the thermal conditions during development. We again used low and high temperature fluctuation treatments and reared individuals in one condition through all egg to pupal stages. At eclosion, we switched half of the individuals in each treatment to the opposite fluctuation condition and, later, measured thermal plasticity of metabolism on adults. We found that temperature conditions experienced during the adult stage, but not egg to pupal stages, affects adult thermal plasticity. However, temperature fluctuations during development affect adult body size, suggesting that some aspects of the adult phenotype are decoupled from previous life stages and others are not. Our data demonstrate that life stages mount different responses to temperature variability and uniquely contribute to the adult phenotype. These findings emphasize the need to broadly integrate the life cycle into studies of phenotypic plasticity and physiology; doing so should enhance our ability to predict organismal responses to rapid global change and inform conservation efforts.« less
  5. Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermalmore »acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.« less