SummaryExamining how morphology, life history and physiology vary along environmental clines can reveal functional insight into adaptations to climate and thus inform predictions about evolutionary responses to global change. Widespread species occurring over latitudinal and altitudinal gradients in seasonal water availability are excellent systems for investigating multivariate adaptation to drought stress.Under common garden conditions, we characterized variation in 27 traits for 52 annual populations of Mimulus guttatus sampled from 10 altitudinal transects. We also assessed variation in the critical photoperiod for flowering and surveyed neutral genetic markers to control for demography when analyzing clinal patterns.Many drought escape (e.g. flowering time) and drought avoidance (e.g. specific leaf area, succulence) traits exhibited geographic or climatic clines, which often remained significant after accounting for population structure. Critical photoperiod and flowering time in glasshouse conditions followed distinct clinal patterns, indicating different aspects of seasonal phenology confer adaptation to unique agents of selection. Although escape and avoidance traits were negatively correlated range-wide, populations from sites with short growing seasons produced both early flowering and dehydration avoidance phenotypes.Our results highlight how abundant genetic variation in the component traits that build multivariate adaptations to drought stress provides flexibility for intraspecific adaptation to diverse climates.

The genetic differentiation of populations in response to local selection pressures has long been studied by evolutionary biologists, but key details about the process remain obscure. How rapidly can local adaptation evolve, how extensive is the process across the genome, and how strong are the opposing forces of natural selection and gene flow? Here, we combine direct measurement of survival and reproduction with whole-genome genotyping of a plant species (Mimulus guttatus) that has recently invaded a novel habitat (the Quarry population). We renovate the classic selection component method to accommodate genomic data and observe selection at SNPs throughout the genome. SNPs showing viability selection in Quarry exhibit elevated divergence from neighboring populations relative to neutral SNPs. We also find that non-significant SNPs exhibit a subtle, but still significant, change in allele frequency towards neighboring populations, a predicted effect of gene flow. Given that the Quarry population is most probably only 30–40 generations old, the alleles conferring local advantage are almost certainly older than the population itself. Thus, local adaptation owes to the recruitment of standing genetic variation.

Sexual reproduction allows transposable elements (TEs) to proliferate, leading to rapid divergence between populations and species. A significant outcome of divergence in the TE landscape is evident in hybrid dysgenic syndromes, a strong form of genomic incompatibility that can arise when (TE) family abundance differs between two parents. When TEs inherited from the father are absent in the mother's genome, TEs can become activated in the progeny, causing germline damage and sterility. Studies in Drosophila indicate that dysgenesis can occur when TEs inherited paternally are not matched with a pool of corresponding TE silencing PIWI-interacting RNAs (piRNAs) provisioned by the female germline. Using the D. virilis syndrome of hybrid dysgenesis as a model, we characterize the effects that divergence in TE profile between parents has on offspring. Overall, we show that divergence in the TE landscape is associated with persisting differences in germline TE expression when comparing genetically identical females of reciprocal crosses and these differences are transmitted to the next generation. Moreover, chronic and persisting TE expression coincides with increased levels of genic piRNAs associated with reduced gene expression. Combined with these effects, we further demonstrate that gene expression is idiosyncratically influenced by differences in the genic piRNA profile of the parents that arise though polymorphic TE insertions. Overall, these results support a model in which early germline events in dysgenesis establish a chronic, stable state of both TE and gene expression in the germline that is maintained through adulthood and transmitted to the next generation. This work demonstrates that divergence in the TE profile is associated with diverse piRNA-mediated transgenerational effects on gene expression within populations.

While native populations are often adapted to historical biotic and abiotic conditions at their home site, populations from other locations in the range may be better adapted to current conditions due to changing climates or extreme conditions in a single year. We examine whether local populations of a widespread species maintain a relative advantage over distant populations that have evolved at sites better matching the current climate. Specifically, we grew lines derived from low-and high-elevation annual populations in California and Oregon of the common monkeyflower (Erythranthe guttata) and conducted phenotypic selection analyses in low-and high-elevation common gardens in Oregon to examine relative fitness and the traits mediating relative fitness. Californian low-elevation populations have the highest relative fitness at the low-elevation site, and Californian high-elevation populations have the highest relative fitness at the high-elevation site. Relative fitness differences are mediated by selection for properly timed transitions to flowering, with selection favoring more rapid growth rates at the low-elevation site and greater vegetative biomass prior to flowering at the high-elevation site. Fitness advantages for Californian plants occur despite incurring higher herbivory at both sites than the native Oregonian plants. Our findings suggest that a lag in adaptation causes maladaptation in extreme years that may be more prevalent in future climates, but local populations still have high growth rates and thus are not yet threatened.

Trichomes, or leaf hairs, are epidermal extensions that take a variety of forms and perform many functions in plants, including herbivore defense. In this study, I document genetically determined variation, within-generation plasticity, and a direct role of trichomes in herbivore defense for Mimulus guttatus. After establishing the relationship between trichomes and herbivory, I test for transgenerational effects of wounding on trichome density and herbivore resistance. Patterns of inter-annual variation in herbivore density and the high cost of plant defense makes plant-herbivore interactions a system in which transgenerational phenotypic plasticity (TPP) is apt to evolve. Here, I demonstrate that parental damage alters offspring trichome density and herbivore resistance in nature. Moreover, this response varies between populations. This is among the first studies to demonstrate that TPP contributes to variation in nature, and also suggests that selection can modify TPP in response to local conditions.