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Abstract PremiseA key goal of evolutionary biologists is to understand how and why genetic variation is partitioned within species. In the yellow monkeyflower,Mimulus guttatus(syn.Erythranthe guttata), coastal perennial populations constitute a single genetically and morphologically differentiated ecotype compared to inlandM. guttatuspopulations. While the coastal ecotype's distinctiveness has now been well documented, there is also environmental variation across the ecotype's range that could drive more continuous differentiation among its component populations. MethodsBased on previous observations of a potential cline within this ecotype, we quantified plant height, among other traits, across coastal perennial accessions from 74 populations in a greenhouse common garden experiment. To evaluate potential drivers of the relationship between trait variation and latitude, we regressed height against multiple climatic factors, including temperature, precipitation, and coastal wind speeds. We also accounted for exposure to the open ocean in all analyses. ResultsMultiple traits were correlated with latitude of origin, but none more than plant height. Height was negatively correlated with latitude, and plants directly exposed to the open ocean were shorter than those protected from coastal winds. Further analyses revealed that height was correlated with climatic factors (precipitation, temperature, and wind speeds) that were autocorrelated with latitude. We hypothesize that one or more of these climatic factors drove the evolution of latitudinal clinal variation within the coastal ecotype. ConclusionsOverall, our study illustrates the complexity of how the distribution of environmental variation can simultaneously drive the evolution of both distinct ecotypesandcontinuous clines within those ecotypes. 

ABSTRACT Chromosomal inversion polymorphisms are ubiquitous across the diversity of diploid organisms and play a significant role in the evolution of adaptations in those species. Inversions are thought to operate as supergenes by trapping adaptive alleles at multiple linked loci through the suppression of recombination. While there is now considerable support for the supergene mechanism of inversion evolution, the extent to which inversions trap pre‐existing adaptive genetic variation versus accumulate new adaptive variants over time remains unclear. In this study, we report new insights into the evolution of a locally adaptive chromosomal inversion polymorphism (inv_chr8A), which contributes to the adaptive divergence between coastal perennial and inland annual ecotypes of the yellow monkeyflower,Mimulus guttatus. This research was enabled by the sequencing, assembly and annotation of new annual and perennial genomes ofM. guttatususing Oxford Nanopore long‐read sequencing technology. In addition to the adaptive inv_chr8A inversion, we identified three other large inversion polymorphisms, including a previously unknown large inversion (inv_chr8B) nested within inv_chr8A. Through population genomic analyses, we determined that the nested inv_chr8B inversion is significantly older than the larger chromosomal inversion in which it resides. We also evaluated the potential role of key candidate genes underlying the phenotypic effects of inv_chr8A. These genes are involved in gibberellin biosynthesis and anthocyanin regulation. Although little evidence was found to suggest that inversion breakpoint mutations drive adaptive phenotypic effects, our findings do support the supergene mechanism of adaptation and suggest it may sometimes involve nested inversions that evolve at different times. 

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. 

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. 

PremiseIdentifying the environmental factors responsible for natural selection across different habitats is crucial for understanding the process of local adaptation in plants. Despite its importance, few studies have successfully isolated the environmental factors driving local adaptation in nature. In this study, we evaluated the agents of selection responsible for local adaptation of the monkeyflowerMimulus guttatusto California's coastal and inland habitats. MethodsWe implemented a manipulative reciprocal transplant experiment at coastal and inland sites, where we excluded aboveground stressors in an effort to elucidate their role in the evolution of local adaptation. ResultsExcluding aboveground stressors, most likely a combination of salt spray and herbivory, completely rescued inland annual plant fitness when transplanted to coastal habitat. The exclosures in inland habitat provided a benefit to the performance of coastal perennial plants. However, the exclosures are unlikely to provide much fitness benefit to the coastal plants at the inland site because of their general inability to flower in time to escape from the summer drought. ConclusionsOur study demonstrates that a distinct set of selective agents (aboveground vs. belowground) are responsible for local adaptation at opposite ends of an environmental gradient. 

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.