An official website of the United States government
Abstract Variation in heat tolerance among populations can determine whether a species is able to cope with ongoing climate change. Such variation may be especially important for ectotherms whose body temperatures, and consequently, physiological processes, are regulated by external conditions.Additionally, differences in body size are often associated with latitudinal clines, thought to be driven by climate gradients. While studies have begun to explore variation in body size and heat tolerance within species, our understanding of these patterns across large spatial scales, particularly regarding the roles of plasticity and genetic differences, remains incomplete.Here, we examine body size, as measured by wing length, and thermal tolerance, as measured by the time to immobilisation at high temperatures (“thermal knockdown”), in populations of the mosquitoAedes sierrensiscollected from across a large latitudinal climate gradient spanning 1300 km (34–44° N).We find that mosquitoes collected from lower latitudes and warmer climates were more tolerant of high temperatures than those collected from higher latitudes and colder climates. Moreover, body size increased with latitude and decreased with temperature, a pattern consistent with James' rule, which appears to be a result of plasticity rather than genetic variation.Our results suggest that warmer environments produce smaller and more thermally tolerant populations.
more »
« less
Thermal plasticity has higher fitness costs among thermally tolerant genotypes of Tigriopus californicus
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
- Award ID(s):
- 2312253
- PAR ID:
- 10565093
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 38
- Issue:
- 7
- ISSN:
- 0269-8463
- Page Range / eLocation ID:
- 1562 to 1577
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract In Mediterranean climates, the timing of seasonal rains determines germination, flowering phenology and fitness. As climate change alters seasonal precipitation patterns, it is important to ask how these changes will affect the phenology and fitness of plant populations. We addressed this question experimentally with the annual plant speciesArabidopsis thaliana.In a first experiment, we manipulated the date of rainfall onset and recorded germination phenology on sand and soil substrates. In a second experiment, we manipulated germination date, growing season length and mid‐season drought to measure their effects on flowering time and fitness. Within each experiment, we manipulated seed dormancy and flowering time using multilocus near‐isogenic lines segregating strong and weak alleles of the seed dormancy geneDOG1and the flowering time geneFRI. We synthesized germination phenology data from the first experiment with fitness functions from the second experiment to project population fitness under different seasonal rainfall scenarios.Germination phenology tracked rainfall onset but was slower and more variable on sand than on soil. Many seeds dispersed on sand in spring and summer delayed germination until the cooler temperatures of autumn. The high‐dormancyDOG1allele also prevented immediate germination in spring and summer. Germination timing strongly affected plant fitness. Fecundity was highest in the October germination cohort and declined in spring germinants. The late floweringFRIallele had lower fecundity, especially in early fall and spring cohorts. Projections of population fitness revealed that: (1) Later onset of autumn rains will negatively affect population fitness. (2) Slow, variable germination on sand buffers populations against fitness impacts of variable spring and summer rainfall. (3) Seasonal selection favours high dormancy and early flowering genotypes in a Mediterranean climate with hot dry summers. The high‐dormancyDOG1allele delayed germination of spring‐dispersed fresh seeds until more favourable early fall conditions, resulting in higher projected population fitness.These findings suggest that Mediterranean annual plant populations are vulnerable to changes in seasonal precipitation, especially in California where rainfall onset is already occurring later. The fitness advantage of highly dormant, early flowering genotypes helps explain the prevalence of this strategy in Mediterranean populations. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
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 thermal 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.more » « less
-
Identifying the genetic basis of local adaptation and fitness trade-offs across environments is a central goal of evolutionary biology. Cold acclimation is an adaptive plastic response for surviving seasonal freezing, and costs of acclimation may be a general mechanism for fitness trade-offs across environments in temperate zone species. Starting with locally adapted ecotypes ofArabidopsis thalianafrom Italy and Sweden, we examined the fitness consequences of a naturally occurring functional polymorphism inCBF2. This gene encodes a transcription factor that is a major regulator of cold-acclimated freezing tolerance and resides within a locus responsible for a genetic trade-off for long-term mean fitness. We estimated the consequences of alternate genotypes ofCBF2on 5-y mean fitness and fitness components at the native field sites by comparing near-isogenic lines with alternate genotypes ofCBF2to their genetic background ecotypes. The effects ofCBF2were validated at the nucleotide level using gene-edited lines in the native genetic backgrounds grown in simulated parental environments. The foreignCBF2genotype in the local genetic background reduced long-term mean fitness in Sweden by more than 10%, primarily via effects on survival. In Italy, fitness was reduced by more than 20%, primarily via effects on fecundity. At both sites, the effects were temporally variable and much stronger in some years. The gene-edited lines confirmed thatCBF2encodes the causal variant underlying this genetic trade-off. Additionally, we demonstrated a substantial fitness cost of cold acclimation, which has broad implications for potential maladaptive responses to climate change.more » « less
-
Summary Plastic responses of plants to their environment vary as a result of genetic differentiation within and among species. To accurately predict rangewide responses to climate change, it is necessary to characterize genotype‐specific reaction norms across the continuum of historic and future climate conditions comprising a species' range.The North American hybrid zone ofPopulus trichocarpaandPopulus balsamiferarepresents a natural system that has been shaped by climate, geography, and introgression. We leverage a dataset containing 44 clonal genotypes from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range. Growth and mortality were measured over 2 yr, enabling us to model reaction norms for each genotype across these tested environments.Species ancestry and intraspecific genomic variation significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade‐off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with moreP. trichocarpaancestry may gain an advantage under warmer climates.Spatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape‐level effects.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/1365-2435.14568
