Impact of Developmental Temperatures On The Repeatability of Thermal Plasticity in Metabolic Rate

Mapping Intimacies ◽

10.32942/osf.io/kp2gd ◽

2021 ◽

Author(s):

Fonti Kar ◽

Shinichi Nakagawa ◽

Daniel W.A. Noble

Keyword(s):

Metabolic Rate ◽

Population Level ◽

Reaction Norm ◽

Thermal Reaction ◽

Reaction Norms ◽

Thermal Plasticity ◽

Credible Intervals ◽

Hot Environments ◽

Plastic Responses ◽

Early Developmental

Phenotypic plasticity is an important mechanism that allows populations to adjust to changing environments. Plastic responses induced by early life experiences can have lasting impacts on how individuals respond to environmental variation later in life (i.e., reversible plasticity). Developmental environments can also influence repeatability of plastic responses thereby altering the capacity for reaction norms to respond to selection. Here, we compared metabolic thermal reaction norms in lizards (Lampropholis delicata) that were incubated at two developmental temperatures (ncold = 26, nhot = 25). We repeatedly measured individual reaction norms across six acute temperatures 10 times over ~3.5 months (nobs = 3,818) to estimate the repeatability of average metabolic rate (intercept) and thermal plasticity (slope). The intercept and the slope of the population-level thermal reaction norm did not change with developmental temperatures. Repeatability of average metabolic rate was, on average, 10% lower in hot incubated lizards and was stable across acute temperatures. The slope of the reaction norm was moderately repeatable (R = 0.44, 95% CI = 0.035 – 0.93) suggesting that individual metabolic rate changed consistently with acute temperature, although credible intervals were quite broad. Importantly, reaction norm repeatability did not depend on early developmental temperature. Our work implies that thermal plasticity has the capacity to evolve, despite there being less consistent variation in metabolic rate under hot environments. This capacity for thermal plasticity to evolve will be increasingly more important for terrestrial ectotherms living in changing climate.

Download Full-text

Thermal reaction norms of key metabolic enzymes reflect divergent physiological and behavioral adaptations of closely related amphipod species

Scientific Reports ◽

10.1038/s41598-021-83748-2 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Lena Jakob ◽

Kseniya P. Vereshchagina ◽

Anette Tillmann ◽

Lorena Rivarola-Duarte ◽

Denis V. Axenov-Gribanov ◽

...

Keyword(s):

Lactate Dehydrogenase ◽

Lake Baikal ◽

Enzyme Activities ◽

Large Scale ◽

Metabolic Enzymes ◽

Thermal Reaction ◽

Reaction Norms ◽

Ecological Niches ◽

Amphipod Species ◽

Thermal Plasticity

AbstractLake Baikal is inhabited by more than 300 endemic amphipod species, which are narrowly adapted to certain thermal niches due to the high interspecific competition. In contrast, the surrounding freshwater fauna is commonly represented by species with large-scale distribution and high phenotypic thermal plasticity. Here, we investigated the thermal plasticity of the energy metabolism in two closely-related endemic amphipod species from Lake Baikal (Eulimnogammarus verrucosus; stenothermal and Eulimnogammarus cyaneus; eurythermal) and the ubiquitous Holarctic amphipod Gammarus lacustris (eurythermal) by exposure to a summer warming scenario (6–23.6 °C; 0.8 °C d−1). In concert with routine metabolic rates, activities of key metabolic enzymes increased strongly with temperature up to 15 °C in E. verrucosus, whereupon they leveled off (except for lactate dehydrogenase). In contrast, exponential increases were seen in E. cyaneus and G. lacustris throughout the thermal trial (Q10-values: 1.6–3.7). Cytochrome-c-oxidase, lactate dehydrogenase, and 3-hydroxyacyl-CoA dehydrogenase activities were found to be higher in G. lacustris than in E. cyaneus, especially at the highest experimental temperature (23.6 °C). Decreasing gene expression levels revealed some thermal compensation in E. cyaneus but not in G. lacustris. In all species, shifts in enzyme activities favored glycolytic energy generation in the warmth. The congruent temperature-dependencies of enzyme activities and routine metabolism in E. verrucosus indicate a strong feedback-regulation of enzymatic activities by whole organism responses. The species-specific thermal reaction norms reflect the different ecological niches, including the spatial distribution, distinct thermal behavior such as temperature-dependent migration, movement activity, and mating season.

Download Full-text

Do Differences in Latitudinal Distributions of Species and Organelle Haplotypes Reflect Thermal Reaction Norms Within the Emiliania/Gephyrocapsa Complex?

Frontiers in Marine Science ◽

10.3389/fmars.2021.785763 ◽

2021 ◽

Vol 8 ◽

Author(s):

Peter von Dassow ◽

Paula Valentina Muñoz Farías ◽

Sarah Pinon ◽

Esther Velasco-Senovilla ◽

Simon Anguita-Salinas

Keyword(s):

Local Adaptation ◽

Coastal Upwelling ◽

Environmental Gradients ◽

Reaction Norm ◽

Emiliania Huxleyi ◽

Thermal Reaction ◽

Reaction Norms ◽

Thermal Niche ◽

Significant Difference ◽

The Difference

The cosmopolitan phytoplankter Emiliania huxleyi contrasts with its closest relatives that are restricted to narrower latitudinal bands, making it interesting for exploring how alternative outcomes in phytoplankton range distributions arise. Mitochondrial and chloroplast haplogroups within E. huxleyi are shared with their closest relatives: Some E. huxleyi share organelle haplogroups with Gephyrocapsa parvula and G. ericsonii which inhabit lower latitudes, while other E. huxleyi share organelle haplogroups with G. muellerae, which inhabit high latitudes. We investigated whether the phylogeny of E. huxleyi organelles reflects environmental gradients, focusing on the Southeast Pacific where the different haplogroups and species co-occur. There was a high congruence between mitochondrial and chloroplast haplogroups within E. huxleyi. Haplogroup II of E. huxleyi is negatively associated with cooler less saline waters, compared to haplogroup I, both when analyzed globally and across temporal variability at the small special scale of a center of coastal upwelling at 30° S. A new mitochondrial haplogroup Ib detected in coastal Chile was associated with warmer waters. In an experiment focused on inter-species comparisons, laboratory-determined thermal reaction norms were consistent with latitudinal/thermal distributions of species, with G. oceanica exhibiting warm thermal optima and tolerance and G. muellerae exhibiting cooler thermal optima and tolerances. Emiliania huxleyi haplogroups I and II tended to exhibit a wider thermal niche compared to the other Gephyrocapsa, but no differences among haplogroups within E. huxleyi were found. A second experiment, controlling for local adaptation and time in culture, found a significant difference between E. huxleyi haplogroups. The difference between I and II was of the expected sign, but not the difference between I and Ib. The differences were small (≤1°C) compared to differences reported previously within E. huxleyi by local adaptation and even in-culture evolution. Haplogroup Ib showed a narrower thermal niche. The cosmopolitanism of E. huxleyi might result from both wide-spread generalist phenotypes and specialist phenotypes, as well as a capacity for local adaptation. Thermal reaction norm differences can well explain the species distributions but poorly explain distributions among mitochondrial haplogroups within E. huxleyi. Perhaps organelle haplogroup distributions reflect historical rather than selective processes.

Download Full-text

Divergence and ontogenetic coupling of larval behaviour and thermal reaction norms in three closely related butterflies

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2010.1398 ◽

2010 ◽

Vol 278 (1703) ◽

pp. 313-320 ◽

Cited By ~ 16

Author(s):

David Berger ◽

Magne Friberg ◽

Karl Gotthard

Keyword(s):

Developmental Plasticity ◽

Larval Growth ◽

State Dependence ◽

Reaction Norm ◽

Thermal Reaction ◽

Reaction Norms ◽

Feeding Strategies ◽

Species Differentiation ◽

Larval Behaviour ◽

Trade Offs

Genetic trade-offs such as between generalist–specialist strategies can be masked by changes in compensatory processes involving energy allocation and acquisition which regulation depends on the state of the individual and its ecological surroundings. Failure to account for such state dependence may thus lead to misconceptions about the trade-off structure and nature of constraints governing reaction norm evolution. Using three closely related butterflies, we first show that foraging behaviours differ between species and change remarkably throughout ontogeny causing corresponding differences in the thermal niches experienced by the foraging larvae. We further predicted that thermal reaction norms for larval growth rate would show state-dependent variation throughout development as a result of selection for optimizing feeding strategies in the respective foraging niches of young and old larvae. We found substantial developmental plasticity in reaction norms that was species-specific and reflected the different ontogenetic niche shifts. Any conclusions regarding constraints on performance curves or species-differentiation in thermal physiology depend on when reaction norms were measured. This demonstrates that standardized estimates at single points in development, or in general, allow variation in only one ecological dimension, may sometimes provide incomplete information on reaction norm constraints.

Download Full-text

Selection on phenotypic plasticity favors thermal canalization

10.1101/2020.06.11.146043 ◽

2020 ◽

Author(s):

Erik I. Svensson ◽

Miguel Gomez-Llano ◽

John T. Waller

Keyword(s):

Climate Change ◽

Sexual Selection ◽

Heat Stress ◽

Natural Selection ◽

Phenotypic Plasticity ◽

Reaction Norm ◽

Thermal Reaction ◽

Ambient Temperatures ◽

Thermal Plasticity ◽

Natural And Sexual Selection

AbstractClimate change affects organisms worldwide with profound ecological and evolutionary consequences, often increasing population extinction risk. Climatic factors can increase the strength, variability or direction of natural selection on phenotypic traits, potentially driving adaptive evolution. Phenotypic plasticity in relation to temperature can allow organisms to maintain fitness in response to increasing temperatures, thereby “buying time” for subsequent genetic adaptation and promoting evolutionary rescue. Although many studies have shown that organisms respond plastically to increasing temperatures, it is unclear if such thermal plasticity is adaptive. Moreover, we know little about how natural and sexual selection operate on thermal reaction norms reflecting such plasticity. Here, we investigate how natural and sexual selection shape phenotypic plasticity in two congeneric and phenotypically similar sympatric insect species. We show that the thermal optima for longevity and mating success differ, suggesting temperature-dependent trade-offs between survival and reproduction. Males in these species have similar thermal reaction norm slopes but have diverged in baseline body temperature (intercepts), being higher for the more northern species. Natural selection favoured reduced thermal reaction norm slopes at high ambient temperatures, suggesting that the current level of thermal plasticity is maladaptive in the context of anthropogenic climate change and that selection now promotes thermal canalization and robustness. Our results show that ectothermic animals also at high latitudes can suffer from overheating and challenge the common view of phenotypic plasticity as being beneficial in harsh and novel environments.Significance StatementOrganisms are increasingly challenged by increasing temperatures due to climate change. In insects, body temperatures are strongly affected by ambient temperatures, and insects are therefore expected to suffer increasingly from heat stress, potentially reducing survival and reproductive success leading to elevated extinction risks. We investigated how ambient temperature affected fitness in two insect species in the temperate zone. Male and female survivorship benefitted more from low temperatures than did reproductive success, which increased with higher temperatures, revealing a thermal conflict between fitness components. Male body temperature plasticity reduced survival, and natural and sexual selection operated on such thermal plasticity. Our results reveal the negative consequences of thermal plasticity and show that these insects have limited ability to buffer heat stress.

Download Full-text

Differences in spatial versus temporal reaction norms for spring and autumn phenological events

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2002713117 ◽

2020 ◽

Vol 117 (49) ◽

pp. 31249-31258

Author(s):

Maria del Mar Delgado ◽

Tomas Roslin ◽

Gleb Tikhonov ◽

Evgeniy Meyke ◽

Coong Lo ◽

...

Keyword(s):

Former Soviet Union ◽

Environmental Gradients ◽

Population Level ◽

Reaction Norm ◽

Population Variation ◽

Reaction Norms ◽

Species Response ◽

Countergradient Variation ◽

Spatial And Seasonal Variation ◽

Phenological Event

For species to stay temporally tuned to their environment, they use cues such as the accumulation of degree-days. The relationships between the timing of a phenological event in a population and its environmental cue can be described by a population-level reaction norm. Variation in reaction norms along environmental gradients may either intensify the environmental effects on timing (cogradient variation) or attenuate the effects (countergradient variation). To resolve spatial and seasonal variation in species’ response, we use a unique dataset of 91 taxa and 178 phenological events observed across a network of 472 monitoring sites, spread across the nations of the former Soviet Union. We show that compared to local rates of advancement of phenological events with the advancement of temperature-related cues (i.e., variation within site over years), spatial variation in reaction norms tend to accentuate responses in spring (cogradient variation) and attenuate them in autumn (countergradient variation). As a result, among-population variation in the timing of events is greater in spring and less in autumn than if all populations followed the same reaction norm regardless of location. Despite such signs of local adaptation, overall phenotypic plasticity was not sufficient for phenological events to keep exact pace with their cues—the earlier the year, the more did the timing of the phenological event lag behind the timing of the cue. Overall, these patterns suggest that differences in the spatial versus temporal reaction norms will affect species’ response to climate change in opposite ways in spring and autumn.

Download Full-text

Individual variation in thermal plasticity and its impact on mass-scaling

10.32942/osf.io/g4z2e ◽

2019 ◽

Author(s):

Fonti Kar ◽

Shinichi Nakagawa ◽

Christopher R Friesen ◽

Daniel W.A. Noble

Keyword(s):

Environmental Change ◽

Metabolic Rate ◽

Population Level ◽

Standard Metabolic Rate ◽

Theoretical Research ◽

Level Variation ◽

Scaling Exponents ◽

Mass Scaling ◽

Thermal Plasticity ◽

Multi Level

1.Physiological processes of individuals can be highly variable and there is mounting evidence that individuals can differ in how they respond to environmental change. The ability for individuals to reversibly adjust their metabolic rate in response to temperature (i.e., metabolic thermal plasticity) may affect mass-scaling at the population level. This process has rarely been investigated before. 2.This study characterised the repeatability of metabolic thermal plasticity and tested how mass-scaling exponents change at different temperatures in the delicate skink (Lampropholis delicata). We repeatedly measured standard metabolic rate of forty-two individuals at six temperatures over the course of three months (N[measurement] = 2418). We explicitly accounted for multi-level variation in our data in order to quantify more precise estimates of mass-scaling exponents at different environmental temperatures.3.Making use of two analytical frameworks, we found that metabolic thermal plasticity was significantly repeatable. Average standard metabolic rate increased as a function of temperature, which was associated with individuals responding more predictably (a decrease in within-individual variance) at higher temperatures. Interpretation of repeatability estimates and cross-temperature correlations varied slightly between the analytic approaches, but they were mostly in agreement. 4.After taking into account within- and among-individual level variation in our data, our estimates for mass-scaling did not change with temperature and were in line with published values for snakes and lizards. This suggests that repeatable plastic responses may contribute to thermal stability of scaling exponents. 5.Our work contributes to our understanding of whether phenotypic plasticity has the capacity to respond to selection which is particularly important for animals coping with rapid environmental change. Acknowledging multi-level variation in body mass and metabolic rate is not only important for comparative studies interested in mass-scaling across the animal kingdom, but also to theoretical research interested using the predictive power of mass-scaling.

Download Full-text

Selection on phenotypic plasticity favors thermal canalization

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2012454117 ◽

2020 ◽

Vol 117 (47) ◽

pp. 29767-29774

Author(s):

Erik I. Svensson ◽

Miguel Gomez-Llano ◽

John T. Waller

Keyword(s):

Climate Change ◽

Sexual Selection ◽

Natural Selection ◽

Phenotypic Plasticity ◽

Reaction Norm ◽

Thermal Reaction ◽

Phenotypic Traits ◽

Common View ◽

Thermal Plasticity ◽

Natural And Sexual Selection

Climate change affects organisms worldwide with profound ecological and evolutionary consequences, often increasing population extinction risk. Climatic factors can increase the strength, variability, or direction of natural selection on phenotypic traits, potentially driving adaptive evolution. Phenotypic plasticity in relation to temperature can allow organisms to maintain fitness in response to increasing temperatures, thereby “buying time” for subsequent genetic adaptation and promoting evolutionary rescue. Although many studies have shown that organisms respond plastically to increasing temperatures, it is unclear if such thermal plasticity is adaptive. Moreover, we know little about how natural and sexual selection operate on thermal reaction norms, reflecting such plasticity. Here, we investigate how natural and sexual selection shape phenotypic plasticity in two congeneric and phenotypically similar sympatric insect species. We show that the thermal optima for longevity and mating success differ, suggesting temperature-dependent trade-offs between survival and reproduction in both sexes. Males in these species have similar thermal reaction norm slopes but have diverged in baseline body temperature (intercepts), being higher for the more northern species. Natural selection favored reduced thermal reaction norm slopes at high ambient temperatures, suggesting that the current level of thermal plasticity is maladaptive in the context of anthropogenic climate change and that selection now promotes thermal canalization and robustness. Our results show that ectothermic animals also at high latitudes can suffer from overheating and challenge the common view of phenotypic plasticity as being beneficial in harsh and novel environments.

Download Full-text

Thermal reaction norms in sperm performance of Atlantic cod (Gadus morhua)

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f10-001 ◽

2010 ◽

Vol 67 (3) ◽

pp. 498-510 ◽

Cited By ~ 28

Author(s):

Craig F. Purchase ◽

Ian A.E. Butts ◽

Alexandre Alonso-Fernández ◽

Edward A. Trippel

Keyword(s):

Phenotypic Plasticity ◽

Gadus Morhua ◽

Atlantic Cod ◽

Swimming Performance ◽

Common Garden ◽

Reaction Norm ◽

Thermal Reaction ◽

Reaction Norms ◽

Experimental Unit ◽

Environment Interaction

Phenotypic plasticity occurs when a genotype produces variable phenotypes under different environments; the shapes of such responses are known as norms of reaction. The genetic scale at which reaction norms can be determined is restricted by the experimental unit that can be exposed to variable environments. This has limited their description beyond the family level in higher organisms, thus hindering our understanding of differences in plasticity at the scale of the individual. Using a three-year common-garden experiment, we quantify reaction norms in sperm performance of individual genotypes within different families of Atlantic cod ( Gadus morhua ). Cod sperm showed phenotypic plasticity in swimming performance across temperatures (3, 6, 11, and 21 °C), but the pattern of the response depended upon how long sperm had been swimming (30, 60, 120, or 180 s), i.e., plasticity in plasticity. Sperm generally swam fastest at intermediate temperatures when first assessed at 30 s after activation. However, a significant genotype × environment interaction was present, indicating inter-individual differences in phenotypic plasticity. To our knowledge, this is the first study to describe variable sperm performance across environmental conditions as a reaction norm. The results have potential theoretical, conservation, and aquaculture implications.

Download Full-text

Advancement in long-distance bird migration through individual plasticity in departure

Nature Communications ◽

10.1038/s41467-021-25022-7 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Jesse R. Conklin ◽

Simeon Lisovski ◽

Phil F. Battley

Keyword(s):

Bird Migration ◽

Population Level ◽

Breeding Site ◽

Environmental Constraints ◽

Adaptive Responses ◽

Long Distance ◽

Direct Observations ◽

Breeding Resources ◽

Plastic Responses

AbstractGlobally, bird migration is occurring earlier in the year, consistent with climate-related changes in breeding resources. Although often attributed to phenotypic plasticity, there is no clear demonstration of long-term population advancement in avian migration through individual plasticity. Using direct observations of bar-tailed godwits (Limosa lapponica) departing New Zealand on a 16,000-km journey to Alaska, we show that migration advanced by six days during 2008–2020, and that within-individual advancement was sufficient to explain this population-level change. However, in individuals tracked for the entire migration (50 total tracks of 36 individuals), earlier departure did not lead to earlier arrival or breeding in Alaska, due to prolonged stopovers in Asia. Moreover, changes in breeding-site phenology varied across Alaska, but were not reflected in within-population differences in advancement of migratory departure. We demonstrate that plastic responses can drive population-level changes in timing of long-distance migration, but also that behavioral and environmental constraints en route may yet limit adaptive responses to global change.

Download Full-text