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Increased aridity and drought associated with climate change are exerting unprecedented selection pressures on plant populations. Whether populations can rapidly adapt, and which life history traits might confer increased fitness under drought, remain outstanding questions.

We utilized a resurrection ecology approach, leveraging dormant seeds from herbarium collections to assess whether populations ofPlantago patagonicafrom the semi‐arid Colorado Plateau have rapidly evolved in response to approximately ten years of intense drought in the region. We quantified multiple traits associated with drought escape and drought resistance and assessed the survival of ancestors and descendants under simulated drought.

Descendant populations displayed a significant shift in resource allocation, in which they invested less in reproductive tissues and relatively more in both above‐ and below‐ground vegetative tissues. Plants with greater leaf biomass survived longer under terminal drought; moreover, even after accounting for the effect of increased leaf biomass, descendant seedlings survived drought longer than their ancestors.

Our results document rapid adaptive evolution in response to climate change in a selfing annual and suggest that shifts in tissue allocation strategies may underlie adaptive responses to drought in arid or semi‐arid environments. This work also illustrates a novel approach, documenting that under specific circumstances, seeds from herbarium specimens may provide an untapped source of dormant propagules for future resurrection experiments.

 

Although chemical defenses and herbivore pressure are widely established as key targets and agents of selection, their roles in local adaptation and determining potential evolutionary responses to changing climates are often neglected. Here, we explore fitness differences between 11 rangewide M. guttatus populations in a field common garden experiment and assess the agents and targets of selection driving relative fitness patterns. We use piecewise structural equation models to disentangle associations between chemical defenses, (phenylpropanoid glycosides; PPGs), and life history traits with herbivory and fitness. While the historical environment of populations is not predictive of fitness differences between populations, >90% of variation in fitness can be predicted by the flowering time and foliar PPG defense arsenal of a population. Piecewise structural equation models indicate that life history traits, particularly earlier flowering time, are strongly and directly linked to fitness. However, herbivory, particularly fruit predation, is also an important agent of selection that creates indirect links between fitness and both chemical defenses and life history traits. Our results emphasize the multivariate nature of the agents and targets of selections in producing adaptation and suggest that future responses to selection must navigate a complex fitness landscape. 

Although chemical defenses and herbivore pressure are widely established as key targets and agents of selection, their roles in local adaptation and determining potential evolutionary responses to changing climates are often neglected. Here, we explore fitness differences between 11 rangewide M. guttatus populations in a field common garden experiment and assess the agents and targets of selection driving relative fitness patterns. We use piecewise structural equation models to disentangle associations between chemical defenses, (phenylpropanoid glycosides; PPGs), and life history traits with herbivory and fitness. While the historical environment of populations is not predictive of fitness differences between populations, >90% of variation in fitness can be predicted by the flowering time and foliar PPG defense arsenal of a population. Piecewise structural equation models indicate that life history traits, particularly earlier flowering time, are strongly and directly linked to fitness. However, herbivory, particularly fruit predation, is also an important agent of selection that creates indirect links between fitness and both chemical defenses and life history traits. Our results emphasize the multivariate nature of the agents and targets of selections in producing adaptation and suggest that future responses to selection must navigate a complex fitness landscape.

 

The North American beaver (Castor canadensis Kuhl) and cottonwoods (Populus spp.) are foundation species, the interactions of which define a much larger community and affect a threatened riparian habitat type. Few studies have tested the effect of these interactions on plant chemistry and a diverse arthropod community. We experimentally examined the impact of beaver foraging on riparian communities by first investigating beaver food preferences for one cottonwood species, Fremont cottonwood (P. fremontii S. Watson), compared to other locally available woody species. We next examined the impact of beaver foraging on twig chemistry and arthropod communities in paired samples of felled and unfelled cottonwood species in northern Arizona (P. fremontii) and southwestern Colorado (narrowleaf cottonwood, P. angustifolia James, and Eastern cottonwood, P. deltoides W. Bartram ex Marshall). Four major patterns emerged: (1) In a cafeteria experiment, beavers chose P. fremontii six times more often than other woody native and exotic species. (2) With two cottonwood species, we found that the nitrogen and salicortin concentrations were up to 45% greater and lignin concentration 14% lower in the juvenile resprout growth of felled trees than the juvenile growth on unfelled trees (six of seven analyses were significant for P. fremontii and four of six were significant for P. angustifolia). (3) With two cottonwood species, arthropod community composition on juvenile branches differed significantly between felled and unfelled trees, with up to 38% greater species richness, 114% greater relative abundance and 1282% greater species diversity on felled trees (six of seven analyses with P. fremontii and four of six analyses with P. angustifolia were significant). The above findings indicate that the highest arthropod diversity is achieved in the heterogenous stands of mixed felled and unfelled trees than in stands of cottonwoods, where beavers are not present. These results also indicate that beaver herbivory changes the chemical composition in 10 out of 13 chemical traits in the juvenile growth of two of the three cottonwood species to potentially allow better defense against future beaver herbivory. (4) With P. deltoides, only one of five analyses in chemistry was significant, and none of the four arthropod community analyses were significant, suggesting that this species and its arthropod community responds differently to beaver. Potential reasons for these differences are unknown. Overall, our findings suggest that in addition to their impact on riparian vegetation, other mammals, birds, and aquatic organisms, beavers also may define the arthropod communities of two of three foundation tree species in these riparian ecosystems. 

Abstract Determining how adaptive combinations of traits arose requires understanding the prevalence and scope of genetic constraints. Frequently observed phenotypic correlations between plant growth, defenses, and/or reproductive timing have led researchers to suggest that pleiotropy or strong genetic linkage between variants affecting independent traits is pervasive. Alternatively, these correlations could arise via independent mutations in different genes for each trait and extensive correlational selection. Here we evaluate these alternatives by conducting a quantitative trait loci (QTL) mapping experiment involving a cross between 2 populations of common monkeyflower (Mimulus guttatus) that differ in growth rate as well as total concentration and arsenal composition of plant defense compounds, phenylpropanoid glycosides (PPGs). We find no evidence that pleiotropy underlies correlations between defense and growth rate. However, there is a strong genetic correlation between levels of total PPGs and flowering time that is largely attributable to a single shared QTL. While this result suggests a role for pleiotropy/close linkage, several other QTLs also contribute to variation in total PPGs. Additionally, divergent PPG arsenals are influenced by a number of smaller-effect QTLs that each underlie variation in 1 or 2 PPGs. This result indicates that chemical defense arsenals can be finely adapted to biotic environments despite sharing a common biochemical precursor. Together, our results show correlations between defense and life-history traits are influenced by pleiotropy or genetic linkage, but genetic constraints may have limited impact on future evolutionary responses, as a substantial proportion of variation in each trait is controlled by independent loci. 

Ecological research has increasingly highlighted the importance of intraspecific variation in shaping the structure and function of communities and ecosystems. Indeed, the effects of intraspecific variation can match or exceed those of interspecific variation. Previous reviews of intraspecific variation in plant traits across heterogeneous environments have focused primarily onmeanphenotypic effects. We propose that a richer and fuller understanding of the ecological causes and consequences of intraspecific variation would be provided by partitioning traitvarianceinto its subcomponents (genetic, environment, genotype by environment interaction).

We used a meta‐analysis of 352 sets of genetic, environment and genotype by environment (G×E) variation estimates from 72 studies of Salicaceae to compare these sources of variation across plant traits (growth, foliar nitrogen, defence compounds), insect herbivore performance metrics (e.g., survival, growth, fecundity) and environmental conditions (e.g., soil nutrients, water, defoliation).

Our findings revealed that variation in levels of defence compounds (both condensed tannins and salicinoids) and insect herbivore performance were primarily genetically determined, while variation in plant growth and foliar nitrogen was more environmentally determined.

Plasticity in plant growth, foliar nitrogen levels and insect herbivore performance varied substantially across different sites (year × location), and nutrient, water and carbon dioxide environments. Plasticity was lowest for chemical defence traits and all traits in contrasting ozone and defoliation environments.

Our quantitative review also revealed several gaps in the literature, including a need for surveying more mature plants, a wider variety of insect herbivore species (e.g., leaf‐galling insects, specialist insects) and underrepresented environmental treatments (e.g., competition, defoliation, disease, light and water availability).

Findings from this analysis highlight the importance of, and patterns within, intraspecific variation with respect to shaping the evolvability and plasticity of traits and governing the interactions of plants and insects.

Aplain language summaryis available for this article.

 

Genetic variation in the chemistry of plant leaves can have ecosystem‐level consequences. Here, we address the hypothesis that genetic variation in foliar condensed tannins along aPopulushybridization gradient influences soil ammonia oxidizers, a group of autotrophic microorganisms that perform the first step of nitrification and are not dependent on carbon derived from plant photosynthesis. Evidence that genetically based plant traits influence the abundance and activity of autotrophic soil microbes would greatly expand the concept of extended plant phenotypes. We found that increasing foliar condensed tannin concentration reduced rates of soil nitrification potential by ~75%, reduced the abundance of ammonia‐oxidizing archaea by ~66%, but had no effect on ammonia‐oxidizing bacteria. Other indices that often drive nitrification rates, including soil total nitrogen, foliar nitrogen, and soilpH, were not significant predictors of either the activity or the abundance of ammonia oxidizers, suggesting genetic variation in foliar condensed tannins may be the dominant regulating factor. These results demonstrate the condensed tannin phenotypes of two different tree species and their naturally occurring hybrids have extended effects on a key ecosystem process and provide evidence for indirect genetic linkages among autotrophs across at least two domains of life.

 

Community genetics aims to understand the effects of intraspecific genetic variation on community composition and diversity, thereby connecting community ecology with evolutionary biology. Thus far, research has shown that plant genetics can underlie variation in the composition of associated communities (e.g., insects, lichen and endophytes), and those communities can therefore be considered as extended phenotypes. This work, however, has been conducted primarily at the plantgenotypelevel and has not identified the key underlying genes. To address this gap, we used genome‐wide association mapping with a population of 445 aspen (Populus tremuloides) genets to identify the genes governing variation in plant traits (defence chemistry, bud phenology, leaf morphology, growth) and insect community composition. We found 49 significant SNP associations in 13Populusgenes that are correlated with chemical defence compounds and insect community traits. Most notably, we identified an early nodulin‐like protein that was associated with insect community diversity and the abundance of interacting foundation species (ants and aphids). These findings support the concept that particular plant traits are the mechanistic link between plant genes and the composition of associated insect communities. In putting the “genes” into “genes to ecosystems ecology”, this work enhances understanding of the molecular genetic mechanisms that underlie plant–insect associations and the consequences thereof for the structure of ecological communities.