An official website of the United States government
Populations often vary in their evolutionary responses to a shared environmental perturbation. A key hurdle in building more predictive models of rapid evolution is understanding this variation—why do some populations and traits evolve while others do not? We combined long-term demographic and environmental data, estimates of quantitative genetic variance components, a resurrection experiment and individual-based evolutionary simulations to gain mechanistic insights into contrasting evolutionary responses to a severe multi-year drought. We examined five traits in two populations of a native California plant, Clarkia xantiana , at three time points over 7 years. Earlier flowering phenology evolved in only one of the two populations, though both populations experienced similar drought severity and demographic declines and were estimated to have considerable additive genetic variance for flowering phenology. Pairing demographic and experimental data with evolutionary simulations suggested that while seed banks in both populations likely constrained evolutionary responses, a stronger seed bank in the non-evolving population resulted in evolutionary stasis. Gene flow through time via germ banks may be an important, underappreciated control on rapid evolution in response to extreme environmental perturbations.
more »
« less
Evolutionary divergence of potential drought adaptations between two subspecies of an annual plant: Are trait combinations facilitated, independent, or constrained?
PremiseWhether 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. MethodsIn 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. ResultsThe 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. ConclusionsClarkia 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
- Award ID(s):
- 1754157
- PAR ID:
- 10453390
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- American Journal of Botany
- Volume:
- 108
- Issue:
- 2
- ISSN:
- 0002-9122
- Format(s):
- Medium: X Size: p. 309-319
- Size(s):
- p. 309-319
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract PremiseSeed germination involves risk; post‐germination conditions might not allow survival and reproduction. Variable, stressful environments favor seeds with germination that avoids risk (e.g., germination in conditions predicting success), spreads risk (e.g., dormancy), or escapes risk (e.g., rapid germination). Germination studies often investigate trait correlations with climate features linked to variation in post‐germination reproductive success. Rarely are long‐term records of population reproductive success available. MethodsSupported by demographic and climate monitoring, we analyzed germination in the California winter‐annualClarkia xantianasubsp.xantiana. Sowing seeds of 10 populations across controlled levels of water potential and temperature, we estimated temperature‐specific base water potential for 20% germination, germination time weighted by water potential above base (hydrotime), and a dormancy index (frequency of viable, ungerminated seeds). Mixed‐effects models analyzed responses to (1) temperature, (2) discrete variation in reproductive success (presence or absence of years with zero seed production by a population), and (3) climate covariates, mean winter precipitation and coefficient of variation (CV) of spring precipitation. For six populations, records enabled analysis with a continuous metric of variable reproduction, the CV of per‐capita reproductive success. ResultsPopulations with more variable reproductive success had higher base water potential and dormancy. Higher base water potential and faster germination occurred at warmer experimental temperatures and in seeds of populations with wetter winters. ConclusionsGeographic variation in seed germination in this species suggests local adaptation to demographic risk and rainfall. High base water potential and dormancy may concentrate germination in years likely to allow reproduction, while spreading risk among years.more » « less
-
Sister taxa with distinct phenotypes often occupy contrasting environments in parapatric ranges, yet we generally do not know whether trait divergence reflects spatially-varying selection. We conducted a reciprocal transplant experiment to test whether selection favors “native phenotypes” in two subspecies of Clarkia xantiana (Onagraceae), an annual plant in California. For four quantitative traits that differ between subspecies, we estimated phenotypic selection in subspecies’ exclusive ranges and their contact zone in two consecutive years. We predicted that in the arid, pollinator-scarce eastern region, selection favors phenotypes of the native subspecies parviflora: small leaves, slow leaf growth, early flowering, and diminutive flowers. In the wetter, pollinator-rich, western range of subspecies xantiana, we expected selection for opposite phenotypes. We investigated pollinator contributions to selection by comparing naturally-pollinated and pollen-supplemented individuals. For reproductive traits and for subspecies xantiana, selection generally matched expectations. The contact zone sometimes showed distinctive selection, and in ssp. parviflora selection sometimes favored non-native phenotypes. Pollinators influenced selection on flowering time but not on flower size. Little temporal variation in selection occurred, possibly because of plastic trait responses across years. Though there were exceptions and some causes of selection remain obscure, phenotypic differentiation between subspecies appears to reflect spatially variable selection.more » « less
-
Flowering plants do not occur alone and often grow in mixed-species communities where pollinator sharing is high and interactions via pollinators can occur at pre- and post-pollination stages. While the causes and consequences of pre-pollination interactions have been well studied little is known about post-pollination interactions via heterospecific pollen (HP) receipt, and even less about the evolutionary implications of these interactions. In particular, the degree to which plants can evolve tolerance mechanisms to the negative effects of HP receipt has received little attention. Here, we aim to fill this gap in our understanding of post-pollination interactions by experimentally testing whether two co-flowering Clarkia species can evolve HP tolerance, and whether tolerance to specific HP ‘genotypes’ (fine-scale local adaptation to HP) occurs. We find that Clarkia species vary in their tolerance to HP effects. Furthermore, conspecific pollen performance and the magnitude of HP effects were related to the recipient's history of exposure to HP in C. xantiana but not in C. speciosa. Specifically, better conspecific pollen performance and smaller HP effects were observed in populations of C. xantiana plants with previous exposure to HP compared to populations without such exposure. These results suggest that plants may have the potential to evolve tolerance mechanisms to HP effects but that these may occur not from the female (stigma, style) but from the male (pollen) perspective, a possibility that is often overlooked. We find no evidence for fine-scale local adaptation to HP receipt. Studies that evaluate the adaptive potential of plants to the negative effects of HP receipt are an important first step in understanding the evolutionary consequences of plant–plant post-pollination interactions. Such knowledge is in turn crucial for deciphering the role of plant–pollinator interactions in driving floral evolution and the composition of co-flowering communities.more » « less
-
Abstract The karrikin (KAR) receptor and several related signaling components have been identified by forward genetic screening, but only a few studies have reported on upstream and downstream KAR signaling components and their roles in drought tolerance. Here, we characterized the functions of KAR UPREGULATED F-BOX 1 (KUF1) in drought tolerance using a reverse genetics approach in Arabidopsis (Arabidopsis thaliana). We observed that kuf1 mutant plants were more tolerant to drought stress than wild-type (WT) plants. To clarify the mechanisms by which KUF1 negatively regulates drought tolerance, we performed physiological, transcriptome, and morphological analyses. We found that kuf1 plants limited leaf water loss by reducing stomatal aperture and cuticular permeability. In addition, kuf1 plants showed increased sensitivity of stomatal closure, seed germination, primary root growth, and leaf senescence to abscisic acid (ABA). Genome-wide transcriptome comparisons of kuf1 and WT rosette leaves before and after dehydration showed that the differences in various drought tolerance-related traits were accompanied by differences in the expression of genes associated with stomatal closure (e.g. OPEN STOMATA 1), lipid and fatty acid metabolism (e.g. WAX ESTER SYNTHASE), and ABA responsiveness (e.g. ABA-RESPONSIVE ELEMENT 3). The kuf1 mutant plants had higher root/shoot ratios and root hair densities than WT plants, suggesting that they could absorb more water than WT plants. Together, these results demonstrate that KUF1 negatively regulates drought tolerance by modulating various physiological traits, morphological adjustments, and ABA responses and that the genetic manipulation of KUF1 in crops is a potential means of enhancing their drought tolerance.more » « less
