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Phytochemical defenses, plant-produced compounds that can deter or slow herbivores, are critical in influencing the interactions between herbivores and their host plants—some of the most diverse and abundant organisms on earth. We discuss the foundational findings and theories related to the direct defense of plants against herbivores by these compounds, as well as continuing research questions in this field. We highlight the costs associated with phytochemical defense production and variation within individual plants in the distribution of phytochemicals, both spatially and temporally. We then discuss coevolutionary theory and the adaptations of herbivores to cope with phytochemical defense compounds. Last, we delve into the incredible diversity of phytochemical compounds, the role of diversity in herbivory, and new ways of measuring and understanding phytochemical diversity. 

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.

 

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. 

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.