skip to main content


Title: Unique drought resistance strategies occur among monkeyflower populations spanning an aridity gradient
Abstract Premise Annual plants often exhibit drought‐escape and avoidance strategies to cope with limited water availability. Determining the extent of variation and factors underlying the evolution of divergent strategies is necessary for determining population responses to more frequent and severe droughts. Methods We leveraged five Mimulus guttatus populations collected across an aridity gradient within manipulative drought and quantitative genetics experiments to examine constitutive and terminal‐drought induced responses in drought resistance traits. Results Populations varied considerably in drought‐escape‐ and drought‐avoidance‐associated traits. The most mesic population demonstrated a unique resource conservative strategy. Xeric populations exhibited extreme plasticity when exposed to terminal drought that included flowering earlier at shorter heights, increasing water‐use efficiency, and shifting C:N ratios. However, plasticity responses also differed between populations, with two populations slowing growth rates and flowering at earlier nodes and another population increasing growth rate. While nearly all traits were heritable, phenotypic correlations differed substantially between treatments and often, populations. Conclusions Our results suggest drought resistance strategies of populations may be finely adapted to local patterns of water availability. Substantial plastic responses suggest that xeric populations can already acclimate to drought through plasticity, but populations not frequently exposed to drought may be more vulnerable.  more » « less
Award ID(s):
2222466 2045643 1920858
PAR ID:
10450505
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
American Journal of Botany
Volume:
110
Issue:
8
ISSN:
0002-9122
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Flowering time and water‐use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time,WUE, andWUEplasticity to drought inArabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) IsWUEplasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions ofA. thalianagrown in well‐watered and season‐ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment.WUEand flowering time were consistently positively genetically correlated.WUEwas correlated withWUEplasticity, but the direction changed between treatments. Selection generally favored early flowering and lowWUE, with drought favoring earlier flowering significantly more than well‐watered conditions. Selection for lowerWUEwas marginally stronger under drought. There were no net fitness costs ofWUEplasticity.WUEplasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation betweenWUEand flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions ofA. thaliana.WUEplasticity may be favored over completely fixed development in environments with periodic drought.

     
    more » « less
  2. Abstract

    Plant populations are limited by resource availability and exhibit physiological trade‐offs in resource acquisition strategies. These trade‐offs may constrain the ability of populations to exhibit fast growth rates under water limitation and high cover of neighbours. However, traits that confer drought tolerance may also confer resistance to competition. It remains unclear how fitness responses to these abiotic conditions and biotic interactions combine to structure grassland communities and how this relationship may change along a gradient of water availability.

    To address these knowledge gaps, we estimated the low‐density growth rates of populations in drought conditions with low neighbour cover and in ambient conditions with average neighbour cover for 82 species in six grassland communities across the Central Plains and Southwestern United States. We assessed the relationship between population tolerance to drought and resistance to competition and determined if this relationship was consistent across a precipitation gradient. We also tested whether population growth rates could be predicted using plant functional traits.

    Across six sites, we observed a positive correlation between low‐density population growth rates in drought and in the presence of interspecific neighbours. This positive relationship was particularly strong in the grasslands of the northern Great Plains but weak in the most xeric grasslands. High leaf dry matter content and a low (more negative) leaf turgor loss point were associated with high population growth rates in drought and with neighbours in most grassland communities.

    Synthesis: A better understanding of how both biotic and abiotic factors impact population fitness provides valuable insights into how grasslands will respond to extreme drought. Our results advance plant strategy theory by suggesting that drought tolerance increases population resistance to interspecific competition in grassland communities. However, this relationship is not evident in the driest grasslands, where above‐ground competition is likely less important. Leaf dry matter content and turgor loss point may help predict which populations will establish and persist based on local water availability and neighbour cover, and these predictions can be used to guide the conservation and restoration of biodiversity in grasslands.

     
    more » « less
  3. Abstract

    Accurately predicting responses to selection is a major goal in biology and important for successful crop breeding in changing environments. However, evolutionary responses to selection can be constrained by such factors as genetic and cross‐environment correlations, linkage, and pleiotropy, and our understanding of the extent and impact of such constraints is still developing. Here, we conducted a field experiment to investigate potential constraints to selection for drought resistance in rice (Oryza sativa) using phenotypic selection analysis and quantitative genetics. We found that traits related to drought response were heritable, and some were under selection, including selection for earlier flowering, which could allow drought escape. However, patterns of selection generally were not opposite under wet and dry conditions, and we did not find individual or closely linked genes that influenced multiple traits, indicating a lack of evidence that antagonistic pleiotropy, linkage, or cross‐environment correlations would constrain selection for drought resistance. In most cases, genetic correlations had little influence on responses to selection, with direct and indirect selection largely congruent. The exception to this was seed mass under drought, which was predicted to evolve in the opposite direction of direct selection due to correlations. Because of this indirect effect on selection on seed mass, selection for drought resistance was not accompanied by a decrease in seed mass, and yield increased with fecundity. Furthermore, breeding lines with high fitness and yield under drought also had high fitness and yield under wet conditions, indicating that there was no evidence for a yield penalty on drought resistance. We found multiple genes in which expression influenced both water use efficiency (WUE) and days to first flowering, supporting a genetic basis for the trade‐off between drought escape and avoidance strategies. Together, these results can provide helpful guidance for understanding and managing evolutionary constraints and breeding stress‐resistant crops.

     
    more » « less
  4. Premise

    Water availability is an important abiotic factor, resulting in differences between plant species growing in xeric and mesic habitats. Species with populations occurring in both habitat types allow examination of whether water availability has acted as a selective force at the intraspecific level. Investigating responses to water availability with a dioecious species allows determination of whether males and females, which often have different physiologies and life histories, respond differently.

    Methods

    An experiment varying water availability was performed under an outdoor rain‐out shelter using plants from two mesic and two xeric populations of the dioecious plantSilene latifolia. Early growth rate, flowering propensity, flower size, and specific leaf area were measured. At the end of the season, the plants were harvested, aboveground and root biomass were measured, and the total number of flowers and fruit produced were counted.

    Results

    Compared to the two mesic populations, plants from the two xeric populations grew more slowly, were less likely to flower, took longer to flower, had thicker leaves, invested less in aboveground biomass and more in root biomass, produced fewer flowers and fruit, but were more likely to live. Many traits exhibited significant habitat type × treatment interactions. Compared to the xeric populations, males—but not females—from mesic populations had less root biomass and greatly reduced their flower production in response to low water availability.

    Conclusions

    Mesic and xeric populations responded in ways congruent with water availability being a selective force for among‐population divergence, especially for males.

     
    more » « less
  5. Premise

    Whether drought‐adaptation mechanisms tend to evolve together, evolve independently, or evolve constrained by genetic architecture is incompletely resolved, particularly for water‐relations traits besides gas exchange. We addressed this issue in two subspecies ofClarkia xantiana(Onagraceae), California winter annuals that separated approximately 65,000 years ago and are adapted, partly by differences in flowering time, to native ranges differing in precipitation.

    Methods

    In these subspecies and in recombinant inbred lines (RILs) from a cross between them, we scored traits related to drought adaptation (timing of seed germination and of flowering, succulence, pressure–volume curve variables) in common environments.

    Results

    The subspecies native to more arid environments (parviflora) exhibited slower seed germination in saturated conditions, earlier flowering, and greater succulence, likely indicating superior drought avoidance, drought escape, and dehydration resistance via water storage. The other subspecies (xantiana) had lower osmotic potential at full turgor and lower water potential at turgor loss, implying superior dehydration tolerance. Genetic correlations among RILs suggest facilitated evolution of some trait combinations and independence of others. Where genetic correlations exist, subspecies differences fell along them, with the exception of differences in succulence and turgor loss point. In that case, subspecies difference overcame genetic correlations, possibly reflecting strong selection and/or antagonistic genetic correlations with other traits.

    Conclusions

    Clarkia xantianasubspecies’ differ in multiple mechanisms of drought adaptation. Genetic architecture generally does not seem to have constrained the evolution of these mechanisms, and it may have facilitated the evolution of some of trait combinations.

     
    more » « less