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Abstract Despite multiple ecological and evolutionary hypotheses that predict patterns of phenotypic relationships between plant growth, reproduction and constitutive and/or induced resistance to herbivores, these hypotheses do not make any predictions about the underlying molecular genetic mechanisms that mediate these relationships.We investigated how divergent plant life‐history strategies in the yellow monkeyflower and a life‐history altering locus,DIV1, influence plasticity of phytochemical herbivory resistance traits in response to attack by two herbivore species with different diet breadth.Life‐history strategy (annual vs. perennial) and theDIV1locus significantly influenced levels of constitutive herbivory resistance, as well as resistance induction following both generalist and specialist herbivory. Perennial plants had higher total levels of univariate constitutive and induced defence than annuals, regardless of herbivore type. Annuals induced less in response to generalist herbivory than did perennials, while induction response was equivalent across the ecotypes for specialist herbivory.The effects of theDIV1locus on levels of constitutive and induced defence were dependent on genetic background, the annual versus perennial haplotype ofDIV1and herbivore identity. The patterns of univariate induction due toDIV1were non‐additive and did not always match expectations based on patterns of divergence for annual/perennial parents. For example, perennial plants had higher levels of constitutive and induced defence than did annuals, but when the annualDIV1was present in the perennial genetic background induction response to herbivory was higher than for the perennial parent lines.Patterns for multivariate defence arsenals generally echoed those of univariate, with annual and perennial monkeyflowers and those with alternative versions ofDIV1differing significantly in constitutive and induced resistance. Like univariate resistance, induced multivariate defence arsenals were affected by herbivore identity.Our results highlight the complexity of the genetic mechanisms underlying plastic response to herbivory. While a genetic locus underlying substantial phenotypic variation in life‐history strategy and constitutive defence also influences defence plasticity, the induction response also depends on genetic background. This result demonstrates the potential for some degree of evolutionary independence between constitutive and induced defence, or induced defence and life‐history strategy, in monkeyflowers. Read the freePlain Language Summaryfor this article on the Journal blog. 

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. 

Abstract PremiseIncreased 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. MethodsWe 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. ResultsDescendant 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. ConclusionsOur 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. 

Abstract 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. 

Arthropod matrices from visual surveys on Populus fremontii, Populus angustifolia and Populus deltoides in Arizona and Colorado. Twig phytochemistry from the same trees. All collected with permission from USFS.