skip to main content


Title: Resource availability alters fitness trade‐offs: implications for evolution in stressful environments
Premise

Industrialization and human activities have elevated temperatures and caused novel precipitation patterns, altering soil moisture and nutrient availability. Predicting evolutionary responses to climate change requires information on the agents of selection that drive local adaptation and influence resource acquisition and allocation. Here, we examined the contribution of nutrient and drought stress to local adaptation, and we tested whether trade‐offs across fitness components constrain or facilitate adaptation under resource stress.

Methods

We exposed 35 families ofBoechera stricta(Brassicaceae) to three levels of water and two levels of nutrient supply in a factorial design in the greenhouse. We sourced maternal families from a broad elevational gradient (2499–3530 m a.s.l.), representing disparate soil moisture and nutrient availability.

Results

Concordant with local adaptation, maternal families from arid, low‐elevation populations had enhanced fecundity under severe drought over those from more mesic, high‐elevation sites. Furthermore, fitness trade‐offs between growth and reproductive success depended on the environmental context. Under high, but not low, nutrient levels, we found a negative phenotypic relationship between the probability of reproduction and growth rate. Similarly, a negative phenotypic association only emerged between fecundity and growth under severe drought stress, not the benign water treatment levels, indicating that stressful resource environments alter the direction of trait correlations. Genetic covariances were broadly concordant with these phenotypic patterns.

Conclusions

Despite high heritabilities in all fitness components across treatments, trade‐offs between growth and reproduction could constrain adaptation to increasing drought stress and novel nutrient levels.

 
more » « less
NSF-PAR ID:
10457695
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
American Journal of Botany
Volume:
107
Issue:
2
ISSN:
0002-9122
Page Range / eLocation ID:
p. 308-318
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Phenotypic differentiation in size and fecundity between native and invasive populations of a species has been suggested as a causal driver of invasion in plants. Local adaptation to novel environmental conditions through a micro‐evolutionary response to natural selection may lead to phenotypic differentiation and fitness advantages in the invaded range. Local adaptation may occur along a stress tolerance trade‐off, favoring individuals that, in benign conditions, shift resource allocation from stress tolerance to increased vigor and fecundity and, therefore, invasiveness. Alternately, the typically disturbed invaded range may select for a plastic, generalist strategy, making phenotypic plasticity the main driver of invasion success. To distinguish between these hypotheses, we performed a field common garden and tested for genetically based phenotypic differentiation, resource allocation shifts in response to water limitation, and local adaptation to the environmental gradient which describes the source locations for native and invasive populations of diffuse knapweed (Centaurea diffusa). Plants were grown in an experimental field in France (naturalized range) under water addition and limitation conditions. After accounting for phenotypic variation arising from environmental differences among collection locations, we found evidence of genetic variation between the invasive and native populations for most morphological and life‐history traits under study. InvasiveC. diffusapopulations produced larger, later maturing, and therefore potentially fitter individuals than native populations. Evidence for local adaptation along a resource allocation trade‐off for water limitation tolerance is equivocal. However, native populations do show evidence of local adaptation to an environmental gradient, a relationship which is typically not observed in the invaded range. Broader analysis of the climatic niche inhabited by the species in both ranges suggests that the physiological tolerances ofC. diffusamay have expanded in the invaded range. This observation could be due to selection for plastic, “general‐purpose” genotypes with broad environmental tolerances.

     
    more » « less
  2. null (Ed.)
    Fungi are important decomposers in terrestrial ecosystems, so their responses to climate change might influence carbon (C) and nitrogen (N) dynamics. We investigated whether growth and activity of fungi under drought conditions were structured by trade-offs among traits in 15 fungal isolates from a Mediterranean Southern California grassland. We inoculated fungi onto sterilized litter that was incubated at three moisture levels (4, 27, and 50% water holding capacity, WHC). For each isolate, we characterized traits that described three potential lifestyles within the newly proposed “YAS” framework: growth yield, resource acquisition, and stress tolerance. Specifically, we measured fungal hyphal length per unit litter decomposition for growth yield; the potential activities of the extracellular enzymes cellobiohydrolase (CBH), β -glucosidase (BG), β -xylosidase (BX), and N-acetyl- β - D -glucosaminidase (NAG) for resource acquisition; and ability to grow in drought vs. higher moisture levels for drought stress tolerance. Although, we had hypothesized that evolutionary and physiological trade-offs would elicit negative relationships among traits, we found no supporting evidence for this hypothesis. Across isolates, growth yield, drought stress tolerance, and extracellular enzyme activities were not significantly related to each other. Thus, it is possible that drought-induced shifts in fungal community composition may not necessarily lead to changes in fungal biomass or decomposer ability in this arid grassland. 
    more » « less
  3. Abstract

    In many organisms, phenotype and fitness are strongly influenced by both current environmental factors and maternal effects. The low genetic variation, high phenotypic plasticity, and telescoping generations seen in aphids permit us to investigate the relative importance and potential interaction of maternal and current environments on phenotype. Although past studies have identified an influence of maternal host plant on offspring phenotype and reproduction in aphids, few have demonstrated the potential for these maternal effects to also interact with the aphid's current environment. By rearing multiple generations ofAphis nerii(Fonscolombe) (Hemiptera: Aphididae) on their host common milkweed,Asclepias syriaca(L.) (Apocynaceae), we tested the relative influence and interaction of both maternal and current environmental effects of crowding and plant quality on aphid body size and reproduction. Our results indicate that aphid body size increased with current plant quality and decreased with aphid density in both generations, with an additional direct, positive relationship between body size and fecundity. We did not find evidence for adaptive maternal effects, e.g., production of fewer, larger, offspring by stressed mothers. Instead, poor maternal environments constrained aphid body size and reproduction. Importantly, these adverse maternal effects were only seen in offspring where subsequent nymph population growth was allowed to increase unchecked, likely reducing available resources. Our study thus demonstrates that the significance of maternal effects in aphid development and reproduction can depend on current resource availability, shaping the phenotype and fecundity of offspring under stressful conditions. Incorporating this framework for how aphid body size and reproduction respond to current and maternal environments may improve predictions for how aphid population growth is impacted by resource limitation across generations.

     
    more » « less
  4. 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
  5. Abstract Plants frequently exhibit tradeoffs between reproduction and growth when resources are limited, and often change these allocation patterns in response to stress. Shorter-lived plants such as annuals tend to allocate relatively more resources toward reproduction when stressed, while longer-lived plants tend to invest more heavily in survival and stress defense. However, severe stress may affect the fitness implications of allocating relatively more resources to reproduction versus stress defense. Increased drought intensity and duration have led to widespread mortality events in coniferous forests. In this review, we ask how potential tradeoffs between reproduction and survival influence the likelihood of drought-induced mortality and species persistence. We propose that trees may exhibit what we call ‘fight or flight’ behaviors under stress. ‘Fight’ behaviors involve greater resource allocation toward survival (e.g., growth, drought-resistant xylem and pest defense). ‘Flight’ consists of higher relative allocation of resources to reproduction, potentially increasing both offspring production and mortality risk for the adult. We hypothesize that flight behaviors increase as drought stress escalates the likelihood of mortality in a given location. 
    more » « less