RESUMO
Morphological novelties, or key innovations, are instrumental to the diversification of the organisms. In plants, one such innovation is the evolution of zygomorphic flowers, which is thought to promote outcrossing and increase flower morphological diversity. We isolated three allelic mutants from two Mimulus species displaying altered floral symmetry and identified the causal gene as the ortholog of Arabidopsis BLADE-ON-PETIOLE. We found that MlBOP and MlCYC2A physically interact and this BOP-CYC interaction module is highly conserved across the angiosperms. Furthermore, MlBOP self-ubiquitinates and suppresses MlCYC2A self-activation. MlCYC2A, in turn, impedes MlBOP ubiquitination. Thus, this molecular tug-of-war between MlBOP and MlCYC2A fine-tunes the expression of MlCYC2A, contributing to the formation of bilateral symmetry in flowers, a key trait in angiosperm evolution.
Assuntos
Flores , Regulação da Expressão Gênica de Plantas , Mimulus , Proteínas de Plantas , Flores/genética , Flores/metabolismo , Mimulus/genética , Mimulus/metabolismo , Proteínas de Plantas/metabolismo , Proteínas de Plantas/genética , Mutação , Ubiquitinação , Ligação Proteica , Fenótipo , Alelos , Proteínas de Ligação a DNA , Fatores de TranscriçãoRESUMO
The emergence of novel traits is often preceded by a potentiation phase, when all the genetic components necessary for producing the trait are assembled. However, elucidating these potentiating factors is challenging. We have previously shown that an anthocyanin-activating R2R3-MYB, STRIPY, triggers the emergence of a distinct foliar pigmentation pattern in the monkeyflower Mimulus verbenaceus. Here, using forward and reverse genetics approaches, we identify three potentiating factors that pattern STRIPY expression: MvHY5, a master regulator of light signaling that activates STRIPY and is expressed throughout the leaf, and two leaf developmental regulators, MvALOG1 and MvTCP5, that are expressed in opposing gradients along the leaf proximodistal axis and negatively regulate STRIPY. These results provide strong empirical evidence that phenotypic novelties can be potentiated through incorporation into preexisting genetic regulatory networks and highlight the importance of positional information in patterning the novel foliar stripe.
Assuntos
Antocianinas , Regulação da Expressão Gênica de Plantas , Pigmentação , Folhas de Planta , Antocianinas/metabolismo , Folhas de Planta/metabolismo , Mimulus/metabolismo , Mimulus/genética , Proteínas de Plantas/metabolismo , Proteínas de Plantas/genética , Fatores de Transcrição/metabolismo , Fatores de Transcrição/genética , FenótipoRESUMO
Characterizing physiological and anatomical changes that underlie rapid evolution following climatic perturbation can broaden our understanding of how climate change is affecting biodiversity. It can also provide evidence of cryptic adaptation despite stasis at higher levels of biological organization. Here, we compared evolutionary changes in populations of Mimulus cardinalis from historically different climates in the north and south of the species' range following an exceptional drought. We grew seeds produced from predrought ancestral plants alongside peak-drought descendants in a common glasshouse and exposed them to wet and dry conditions. Before the drought, northern ancestral populations expressed traits contributing to drought escape, while southern ancestral populations expressed drought avoidance. Following the drought, both regions evolved to reduce water loss and maintain photosynthesis in dry treatments (drought avoidance), but via different anatomical alterations in stomata, trichomes, and palisade mesophyll. Additionally, southern populations lost the ability to take advantage of wet conditions. These results reveal rapid evolution towards drought avoidance at an anatomical level following an exceptional drought, but suggest that differences in the mechanisms between regions incur different trade-offs. This sheds light on the importance of characterizing underlying mechanisms for downstream life-history and macromorphological traits.
Assuntos
Evolução Biológica , Secas , Fotossíntese , Folhas de Planta , Folhas de Planta/fisiologia , Folhas de Planta/anatomia & histologia , Mimulus/fisiologia , Mimulus/genética , Mimulus/anatomia & histologia , Água/fisiologia , Estômatos de Plantas/fisiologia , Estômatos de Plantas/anatomia & histologiaRESUMO
Stebbins hypothesized that selfing lineages are evolutionary dead ends because they lack adaptive potential. While selfing populations often possess limited nucleotide variability compared with closely related outcrossers, reductions in the genetic variability of quantitative characters remain unclear, especially for key traits determining selfing rates. Yellow monkeyflower (Mimulus guttatus) populations generally outcross and maintain extensive quantitative genetic variation in floral traits. Here, we study the Joy Road population (Bodega Bay, CA, USA) of M. guttatus, where individuals exhibit stigma-anther distances (SAD) typical of primarily selfing monkeyflowers. We show that this population is closely related to nearby conspecifics on the Pacific Coast with a modest 33% reduction in genome-wide variation compared with a more highly outcrossing population. A five-generation artificial selection experiment challenged the hypothesis that the Joy Road population harbours comparatively low evolutionary potential in stigma-anther distance, a critical determinant of selfing rate in Mimulus. Artificial selection generated a weak phenotypic response, with low realized heritabilities (0.020-0.028) falling 84% below those measured for floral characters in more highly outcrossing M. guttatus. These results demonstrate substantial declines in evolutionary potential with a transition toward selfing. Whether these findings explain infrequent reversals to outcrossing or general limits on adaptation in selfers requires further investigation.
Assuntos
Flores , Mimulus , Seleção Genética , Mimulus/genética , Mimulus/fisiologia , Flores/fisiologia , Evolução Biológica , Polinização , Variação Genética , California , Autofertilização , FenótipoRESUMO
Polyploidy occurs across the tree of life and is especially common in plants. Because newly formed cytotypes are often incompatible with their progenitors, polyploidy is also said to trigger "instantaneous" speciation. If a polyploid can self-fertilize or reproduce asexually, it is even possible for one individual to produce an entirely new lineage, but how often this scenario occurs is unclear. Here, we investigate the evolutionary history of the wild allotetraploid Mimulus sookensis, which was formed through hybridization between self-compatible, diploid species in the Mimulus guttatus complex. We generate a chromosome-scale reference assembly for M. sookensis and define its distinct subgenomes. Despite previous reports suggesting multiple origins of this highly selfing polyploid, we discover patterns of population genomic variation that provide unambiguous support for a single origin. One M. sookensis subgenome is clearly derived from the selfer Mimulus nasutus, which organellar variation suggests is the maternal progenitor. The ancestor of the other subgenome is less certain, but it shares variation with both Mimulus decorus and M. guttatus, two outcrossing diploids with geographic ranges that overlap broadly with M. sookensis. This study establishes M. sookensis as an example of instantaneous speciation, likely facilitated by the polyploid's predisposition to self-fertilize.
Assuntos
Genoma de Planta , Mimulus , Mimulus/genética , Variação Genética , Poliploidia , Hibridização Genética , Evolução Molecular , Evolução Biológica , TetraploidiaRESUMO
Gene expression can be influenced by genetic variants that are closely linked to the expressed gene (cis eQTLs) and variants in other parts of the genome (trans eQTLs). We created a multiparental mapping population by sampling genotypes from a single natural population of Mimulus guttatus and scored gene expression in the leaves of 1,588 plants. We find that nearly every measured gene exhibits cis regulatory variation (91% have FDR < 0.05). cis eQTLs are usually allelic series with three or more functionally distinct alleles. The cis locus explains about two thirds of the standing genetic variance (on average) but varies among genes and tends to be greatest when there is high indel variation in the upstream regulatory region and high nucleotide diversity in the coding sequence. Despite mapping over 10,000 trans eQTL / affected gene pairs, most of the genetic variance generated by trans acting loci remains unexplained. This implies a large reservoir of trans acting genes with subtle or diffuse effects. Mapped trans eQTLs show lower allelic diversity but much higher genetic dominance than cis eQTLs. Several analyses also indicate that trans eQTLs make a substantial contribution to the genetic correlations in expression among different genes. They may thus be essential determinants of "gene expression modules," which has important implications for the evolution of gene expression and how it is studied by geneticists.
Assuntos
Alelos , Regulação da Expressão Gênica de Plantas , Mimulus , Locos de Características Quantitativas , Mimulus/genética , Mapeamento Cromossômico , Genótipo , Variação Genética , Genoma de Planta , Genes de PlantasRESUMO
Hybridization is common in flowering plants and is believed to be an important force driving adaptation and speciation. The flowers of hybrids often exhibit new trait combinations, which, theoretically, could attract new species of pollinators. In this study, we found that the hybrids between a hummingbird-pollinated species Mimulus cardinalis and a self-pollinated species Mimulus parishii attract bumblebees (Bombus impatiens), a pollinator not attracted to either of the progenitor species. This novel attraction is explained by new combinations of floral traits in hybrids, including, most importantly, petal color, in addition to nectar concentration and corolla size. To understand how petal color variation is perceived by bumblebees, we performed reflectance spectroscopy and multispectral imaging to model the flower appearance in bee vision. This analysis showed that color variation would impact the ease of detection. We also found that YUP, the genetic locus responsible for a large portion of floral color variation and previously shown to be important in bee interactions with other Mimulus species, also played an important role in this novel attraction. These results together suggest that the attraction of new pollinators to hybrid plants could be an underexplored avenue for pollinator shift and speciation.
Assuntos
Mimulus , Abelhas , Animais , Mimulus/genética , Polinização , Plantas/genética , Flores/genética , Loci GênicosRESUMO
Climate anomalies are increasing and posing strong selection, which can lead to rapid evolution. This is occurring on a backdrop of interannual variability that might weaken or even reverse selection. However, the effect of interannual climatic variability on rapid evolution is rarely considered. We study the climatic differences that contribute to rapid evolution throughout a 7-year period, encompassing a severe drought across 12 populations of Mimulus cardinalis (scarlet monkeyflower). Plants were grown in a common greenhouse environment under wet and dry treatments, where specific leaf area and date of flowering were measured. We examine the association between trait values and different climate metrics at different time periods, including the collection year, prior years, and cumulative metrics across sequential years. Of the climatic variables we assessed, we find that anomalies in mean annual precipitation best describe trait differences over our study period. Past climates, of 1-2 years prior, are often related to trait values in a conflicting direction to collection-year climate. Uncovering these complex climatic impacts on evolution is critical to better predict and interpret the impacts of climate change.
Assuntos
Evolução Biológica , Mudança Climática , Secas , Mimulus , Mimulus/genética , Mimulus/fisiologia , Fenótipo , Clima , Flores/fisiologia , Flores/genéticaRESUMO
The evolution of postzygotic isolation is thought to be a key step in maintaining species boundaries upon secondary contact, yet the dynamics and persistence of hybrid incompatibilities in naturally hybridizing species are not well understood. Here, we explore these issues using genetic mapping in three independent populations of recombinant inbred lines between naturally hybridizing monkeyflowers, Mimulus guttatus and Mimulus nasutus, from the sympatric Catherine Creek population. We discover that the three M. guttatus founders differ dramatically in admixture history, with nearly a quarter of one founder's genome introgressed from M. nasutus. Comparative genetic mapping in the three RIL populations reveals three new putative inversions, each one segregating among the M. guttatus founders, two due to admixture. We find strong, genome-wide transmission ratio distortion in all RILs, but patterns are highly variable among the three populations. At least some of this distortion appears to be explained by epistatic selection favouring parental genotypes, but tests of inter-chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky-Muller incompatibilities. We also map several genetic loci for hybrid pollen viability, including two interacting pairs that coincide with peaks of distortion. Remarkably, even with this limited sample of three M. guttatus lines, we discover abundant segregating variation for hybrid incompatibilities with M. nasutus, suggesting this population harbours diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities between Mimulus species persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system.
Assuntos
Mimulus , Mimulus/genética , Hibridização Genética , Mapeamento Cromossômico , Genótipo , Desequilíbrio de LigaçãoRESUMO
PREMISE: Duplicated genes (paralogs) are abundant in plant genomes, and their retention may influence the function of genetic programs and contribute to evolutionary novelty. How gene duplication affects genetic modules and what forces contribute to paralog retention are outstanding questions. The CYCLOIDEA(CYC)-dependent flower symmetry program is a model for understanding the evolution of gene duplication, providing multiple examples of paralog partitioning and novelty. However, a novel CYC gene lineage duplication event near the origin of higher core Lamiales (HCL) has received little attention. METHODS: To understand the evolutionary fate of duplicated HCL CYC2 genes, we determined the effects on flower symmetry by suppressing MlCYC2A and MlCYC2B expression using RNA interference (RNAi). We determined the phenotypic effects on flower symmetry in single- and double-silenced backgrounds and coupled our functional analyses with expression surveys of MlCYC2A, MlCYC2B, and a putative downstream RADIALIS (MlRAD5) ortholog. RESULTS: MlCYC2A and MlCYC2B jointly contribute to bilateral flower symmetry. MlCYC2B exhibits a clear dorsal flower identity function and may additionally function in carpel development. MlCYC2A functions in establishing dorsal petal shape. Further, our results suggest an MlCYC2A-MlCYC2B regulatory interaction, which may affect pathway homeostasis. CONCLUSIONS: Our results suggest that CYC paralogs specific to higher core Lamiales may be selectively retained for their joint contribution to bilateral flower symmetry, similar to the independently derived CYC paralogs in the Lamiales model for bilateral flower symmetry research, Antirrhinum majus (snapdragon).
Assuntos
Antirrhinum , Lamiales , Mimulus , Filogenia , Mimulus/genética , Genes de Plantas , Proteínas de Plantas/genética , Lamiales/genética , Flores , Antirrhinum/genética , Antirrhinum/metabolismo , Regulação da Expressão Gênica de PlantasRESUMO
The floras on chemically and physically challenging soils, such as gypsum, shale, and serpentine, are characterized by narrowly endemic species. The evolution of edaphic endemics may be facilitated or constrained by genetic correlations among traits contributing to adaptation and reproductive isolation across soil boundaries. The yellow monkeyflowers in the Mimulus guttatus species complex are an ideal system in which to examine these evolutionary patterns. To determine the genetic basis of adaptive and prezygotic isolating traits, we performed genetic mapping experiments with F2 hybrids derived from a cross between a serpentine endemic, M. nudatus, and its close relative M. guttatus. Few large effect and many small effect QTL contribute to interspecific divergence in life history, floral, and leaf traits, and a history of directional selection contributed to trait divergence. Loci contributing to adaptive traits and prezygotic reproductive isolation overlap, and their allelic effects are largely in the direction of species divergence. These loci contain promising candidate genes regulating flowering time and plant organ size. Together, our results suggest that genetic correlations among traits can facilitate the evolution of adaptation and speciation and may be a common feature of the genetic architecture of divergence between edaphic endemics and their widespread relatives.
Assuntos
Mimulus , Mimulus/genética , Locos de Características Quantitativas , Fenótipo , Mapeamento Cromossômico , Solo/química , Flores/genéticaRESUMO
The origin of phenotypic novelty is a perennial question of genetics and evolution. To date, few studies of biological pattern formation specifically address multi-generational aspects of inheritance and phenotypic novelty. For quantitative traits influenced by many segregating alleles, offspring phenotypes are often intermediate to parental values. In other cases, offspring phenotypes can be transgressive to parental values. For example, in the model organism Mimulus (monkeyflower), the offspring of parents with solid-colored petals exhibit novel spotted petal phenotypes. These patterns are controlled by an activator-inhibitor gene regulatory network with a small number of loci. Here we develop and analyze a model of hybridization and pattern formation that accounts for the inheritance of a diploid gene regulatory network composed of either homozygous or heterozygous alleles. We find that the resulting model of multi-generational Turing-type pattern formation can reproduce transgressive petal phenotypes similar to those observed in Mimulus. The model gives insight into how non-patterned parent phenotypes can yield phenotypically transgressive, patterned offspring, aiding in the development of empirically testable hypotheses.
Assuntos
Mimulus , Mimulus/genética , Evolução Biológica , Conceitos Matemáticos , Modelos Biológicos , Fenótipo , Hibridização GenéticaRESUMO
The evolution of genomic incompatibilities causing postzygotic barriers to hybridization is a key step in species divergence. Incompatibilities take 2 general forms-structural divergence between chromosomes leading to severe hybrid sterility in F1 hybrids and epistatic interactions between genes causing reduced fitness of hybrid gametes or zygotes (Dobzhansky-Muller incompatibilities). Despite substantial recent progress in understanding the molecular mechanisms and evolutionary origins of both types of incompatibility, how each behaves across multiple generations of hybridization remains relatively unexplored. Here, we use genetic mapping in F2 and recombinant inbred line (RIL) hybrid populations between the phenotypically divergent but naturally hybridizing monkeyflowers Mimulus cardinalis and M. parishii to characterize the genetic basis of hybrid incompatibility and examine its changing effects over multiple generations of experimental hybridization. In F2s, we found severe hybrid pollen inviability (<50% reduction vs parental genotypes) and pseudolinkage caused by a reciprocal translocation between Chromosomes 6 and 7 in the parental species. RILs retained excess heterozygosity around the translocation breakpoints, which caused substantial pollen inviability when interstitial crossovers had not created compatible heterokaryotypic configurations. Strong transmission ratio distortion and interchromosomal linkage disequilibrium in both F2s and RILs identified a novel 2-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction eliminated 3 of the expected 9 F2 genotypic classes via F1 gamete loss without detectable effects on the pollen number or viability of F2 double heterozygotes. Along with the mapping of numerous milder incompatibilities, these key findings illuminate the complex genetics of plant hybrid breakdown and are an important step toward understanding the genomic consequences of natural hybridization in this model system.
Assuntos
Mimulus , Mimulus/genética , Mapeamento Cromossômico , Hibridização Genética , Locos de Características Quantitativas , GenômicaRESUMO
PREMISE: Annual plants often exhibit drought-escape and avoidance strategies to cope with limited water availability. Determining the extent of variation and factors underlying the evolution of divergent strategies is necessary for determining population responses to more frequent and severe droughts. METHODS: We leveraged five Mimulus guttatus populations collected across an aridity gradient within manipulative drought and quantitative genetics experiments to examine constitutive and terminal-drought induced responses in drought resistance traits. RESULTS: Populations varied considerably in drought-escape- and drought-avoidance-associated traits. The most mesic population demonstrated a unique resource conservative strategy. Xeric populations exhibited extreme plasticity when exposed to terminal drought that included flowering earlier at shorter heights, increasing water-use efficiency, and shifting C:N ratios. However, plasticity responses also differed between populations, with two populations slowing growth rates and flowering at earlier nodes and another population increasing growth rate. While nearly all traits were heritable, phenotypic correlations differed substantially between treatments and often, populations. CONCLUSIONS: Our results suggest drought resistance strategies of populations may be finely adapted to local patterns of water availability. Substantial plastic responses suggest that xeric populations can already acclimate to drought through plasticity, but populations not frequently exposed to drought may be more vulnerable.
Assuntos
Mimulus , Mimulus/genética , Resistência à Seca , Fenótipo , Secas , ÁguaRESUMO
Barriers to reproduction are often how progress in speciation is measured. Nonetheless, an unresolved question concerns the extent to which reproductive barriers diminish gene flow between incipient species. The Sierra Nevada foothill endemic Mimulus glaucescens and the widespread M. guttatus are considered distinct species based on striking differences in vegetative morphology, but barriers to reproduction have not been previously identified, nor has gene flow between species been characterized. Here, we examined 15 potential reproductive barriers within a Northern California area of broad sympatry. Most barriers, with the exception of ecogeographic isolation, were weak or absent, and total isolation for each species was incomplete. Population genomic analyses of range-wide and broadly sympatric accessions revealed extensive gene flow between these taxa, particularly in sympatry. Despite widespread introgression, Mimulus glaucescens, emerged as monophyletic and largely comprised a single ancestry that was found at intermediate frequency within M. guttatus. This result, along with observed ecological and phenotypic differentiation, suggests that natural selection may contribute to the maintenance of distinct phenotypic forms in the earliest stages of speciation. Integrating estimates of barrier strength with direct estimates of gene flow can strengthen a more nuanced interpretation of the process of speciation in natural communities.
Assuntos
Mimulus , Isolamento Reprodutivo , Mimulus/genética , Fluxo Gênico , Hibridização Genética , Reprodução , Simpatria , Especiação GenéticaRESUMO
Taxon-specific small RNA loci are widespread in eukaryotic genomes, yet their role in lineage-specific adaptation, phenotypic diversification, and speciation is poorly understood. Here, we report that a speciation locus in monkeyflowers (Mimulus), YELLOW UPPER (YUP), contains an inverted repeat region that produces small interfering RNAs (siRNAs) in a phased pattern. Although the inverted repeat is derived from a partial duplication of a protein-coding gene that is not involved in flower pigmentation, one of the siRNAs targets and represses a master regulator of floral carotenoid pigmentation. YUP emerged with two protein-coding genes that control other aspects of flower coloration as a "superlocus" in a subclade of Mimulus and has contributed to subsequent phenotypic diversification and pollinator-mediated speciation in the descendant species.
Assuntos
Carotenoides , Flores , Regulação da Expressão Gênica no Desenvolvimento , Regulação da Expressão Gênica de Plantas , Mimulus , Pigmentação , RNA Interferente Pequeno , Carotenoides/metabolismo , Flores/genética , Flores/crescimento & desenvolvimento , Mimulus/genética , Mimulus/crescimento & desenvolvimento , Pigmentação/genética , RNA Interferente Pequeno/genética , Loci GênicosRESUMO
The expression of phased small interfering RNAs caused monkeyflower color evolution.
Assuntos
Flores , Mimulus , Pigmentação , RNA Interferente Pequeno , Flores/crescimento & desenvolvimento , Flores/metabolismo , Pigmentação/genética , RNA Interferente Pequeno/genética , RNA Interferente Pequeno/metabolismo , Mimulus/genética , Mimulus/crescimento & desenvolvimentoRESUMO
Spatially and temporally varying selection can maintain genetic variation within and between populations, but it is less well known how these forces influence divergence between closely related species. We identify the interaction of temporal and spatial variation in selection and their role in either reinforcing or eroding divergence between two closely related Mimulus species. Using repeated reciprocal transplant experiments with advanced generation hybrids, we compare the strength of selection on quantitative traits involved in adaptation and reproductive isolation in Mimulus guttatus and Mimulus laciniatus between two years with dramatically different water availability. We found strong divergent habitat-mediated selection on traits in the direction of species differences during a drought in 2013, suggesting that spatially varying selection maintains species divergence. However, a relaxation in divergent selection on most traits in an unusually wet year (2019), including flowering time, which is involved in pre-zygotic isolation, suggests that temporal variation in selection may weaken species differences. Therefore, we find evidence that temporally and spatially varying selection may have opposing roles in mediating species boundaries. Given our changing climate, future growing seasons are expected to be more similar to the dry year, suggesting that in this system climate change may actually increase species divergence.
Assuntos
Mimulus , Mimulus/genética , Flores/genética , Fenótipo , Adaptação Fisiológica/genética , Isolamento ReprodutivoRESUMO
Understanding the phenotypic and genetic architecture of reproductive isolation is a long-standing goal of speciation research. In several systems, large-effect loci contributing to barrier phenotypes have been characterized, but such causal connections are rarely known for more complex genetic architectures. In this study, we combine "top-down" and "bottom-up" approaches with demographic modelling toward an integrated understanding of speciation across a monkeyflower hybrid zone. Previous work suggests that pollinator visitation acts as a primary barrier to gene flow between two divergent red- and yellow-flowered ecotypes of Mimulus aurantiacus. Several candidate isolating traits and anonymous single nucleotide polymorphism loci under divergent selection have been identified, but their genomic positions remain unknown. Here, we report findings from demographic analyses that indicate this hybrid zone formed by secondary contact, but that subsequent gene flow was restricted by widespread barrier loci across the genome. Using a novel, geographic cline-based genome scan, we demonstrate that candidate barrier loci are broadly distributed across the genome, rather than mapping to one or a few "islands of speciation." Quantitative trait locus (QTL) mapping reveals that most floral traits are highly polygenic, with little evidence that QTL colocalize, indicating that most traits are genetically independent. Finally, we find little evidence that QTL and candidate barrier loci overlap, suggesting that some loci contribute to other forms of reproductive isolation. Our findings highlight the challenges of understanding the genetic architecture of reproductive isolation and reveal that barriers to gene flow other than pollinator isolation may play an important role in this system.
Assuntos
Mimulus , Mimulus/genética , Mapeamento Cromossômico , Isolamento Reprodutivo , Fenótipo , Ecótipo , Especiação GenéticaRESUMO
The origin of phenotypic novelty is one of the most challenging problems in evolutionary biology. Although genetic regulatory network rewiring or co-option has been widely recognised as a major contributor, in most cases how such genetic rewiring/co-option happens is completely unknown. We have studied a novel foliar pigmentation pattern that evolved recently in the monkeyflower species Mimulus verbenaceus. Through genome-wide association tests using wild-collected samples, experimental crosses of laboratory inbred lines, gene expression analyses, and functional assays, we identified an anthocyanin-activating R2R3-MYB gene, STRIPY, as the causal gene triggering the emergence of the discrete, mediolateral anthocyanin stripe in the M. verbenaceus leaf. Chemical mutagenesis revealed the existence of upstream activators and repressors that form a 'hidden' prepattern along the leaf proximodistal axis, potentiating the unique expression pattern of STRIPY. Population genomics analyses did not reveal signatures of positive selection, indicating that nonadaptive processes may be responsible for the establishment of this novel trait in the wild. This study demonstrates that the origin of phenotypic novelty requires at least two separate phases, potentiation and actualisation. The foliar stripe pattern of M. verbenaceus provides an excellent platform to probe the molecular details of both processes in future studies.