Genome-wide association mapping of transcriptome variation in Mimulus guttatus indicates differing patterns of selection on cis- versus trans-acting mutations

We measured the floral bud transcriptome of 151 fully sequenced lines of Mimulus guttatus from one natural population. Thousands of single nucleotide polymorphisms (SNPs) are implicated as transcription regulators, but there is a striking difference in the Allele Frequency Spectrum (AFS) of cis-acting and trans-acting mutations. Cis-SNPs have intermediate frequencies (consistent with balancing selection) while trans-SNPs exhibit a rare-alleles model (consistent with purifying selection). This pattern only becomes clear when transcript variation is normalized on a gene-to-gene basis. If a global normalization is applied, as is typically in RNAseq experiments, asymmetric transcript distributions combined with “rarity disequilibrium” produce a super-abundance of false positives for trans-acting SNPs. To explore the cause of purifying selection on trans-acting mutations, we identified gene expression modules as sets of co-expressed genes. The extent to which trans-acting mutations influence modules is a strong predictor of allele frequency. Mutations altering expression of genes with high “connectedness” (those that are highly predictive of the representative module expression value) have the lowest allele frequency. The expression modules can also predict whole-plant traits such as flower size. We find that a substantial portion of the genetic (co)variance among traits can be described as an emergent property of genetic effects on expression modules.

Population genomic consequences of novel life history and mating system adaptation to a geothermal soil mosaic in yellow monkeyflowers (Mimulus guttatus)

Local selection can promote phenotypic divergence despite gene flow across habitat mosaics, but adaptation itself may generate substantial barriers to genetic exchange. In plants, life-history, phenology, and mating system divergence have been particularly proposed to promote genetic differentiation in sympatry. In this study, we investigate phenotypic and genetic variation in Mimulus guttatus (yellow monkeyflowers) across a geothermal soil mosaic in Yellowstone National Park (YNP). Plants from thermal annual and nonthermal perennial habitats were heritably differentiated for life history and mating system traits, consistent with local adaptation to the ephemeral thermal-soil growing season. However, genome-wide genetic variation primarily clustered plants by geographic region, with little variation sorting by habitat. The one exception was an extreme thermal population also isolated by a 200m geographical gap. Individual inbreeding coefficients (FIS) were higher (and predicted by trait variation) in annual plants and annual pairs showed greater isolation by distance at local (<1km) scales. Finally, YNP adaptation does not re-use a widespread inversion polymorphism diagnostic of annual vs. perennial M. guttatus range-wide, suggesting a novel genetic mechanism. Overall, this work suggests that life history and mating system adaptation strong enough to shape individual mating patterns does not necessarily generate incipient speciation without geographical barriers.

Genome-wide association mapping of transcriptome variation in Mimulus guttatus indicates differing patterns of selection on cis- versus trans-acting mutations

We measured the floral bud transcriptome of 151 fully sequenced lines of Mimulus guttatus from one natural population. Thousands of single nucleotide polymorphisms (SNPs) are implicated as transcription regulators, but there is a striking difference in the Allele Frequency Spectrum (AFS) of cis-acting and trans-acting mutations. Cis-SNPs have intermediate frequencies (consistent with balancing selection) while trans-SNPs exhibit a rare-alleles model (consistent with purifying selection). This pattern only becomes clear when transcript variation is normalized on a gene-to-gene basis. If a global normalization is applied, as is typically in RNAseq experiments, asymmetric transcript distributions combined with rarity disequilibrium produce a super-abundance of false positives for trans-acting SNPs. To explore the cause of purifying selection on trans-acting mutations, we identified gene expression modules as sets of co-expressed genes. The extent to which trans-acting mutations influence modules is a strong predictor of allele frequency. Mutations altering expression of genes with high connectedness (those that are highly predictive of the representative module expression value) have the lowest allele frequency. The expression modules can also predict whole-plant traits such as flower size. We find that a substantial portion of the genetic (co)variance among traits can be described as an emergent property of genetic effects on expression modules.

The genetic architecture and evolution of life-history divergence among perennials in the Mimulus guttatus species complex

Ecological divergence is a fundamental source of phenotypic diversity between closely related species, yet the genetic architecture of most ecologically relevant traits is poorly understood. Differences in elevation can impose substantial divergent selection on both complex, correlated suites of traits (such as life-history), as well as novel adaptations. We use the Mimulus guttatus species complex to assess if the divergence in elevation is accompanied by trait divergence in a group of closely related perennials and determine the genetic architecture of this divergence. We find that divergence in elevation is associated with differences in life-history, as well as a unique trait, the production of rhizomes. The divergence between two perennials is largely explained by few mid-to-large effect quantitative trait loci (QTLs). However, the presence of QTLs with correlated, but opposing effects on multiple traits leads to some hybrids with transgressive trait combinations. Lastly, we find that the genetic architecture of the ability to produce rhizomes changes through development, wherein most hybrids produce rhizomes, but only later in development. Our results suggest that elevational differences may shape life-history divergence between perennials, but aspects of the genetic architecture of divergence may have implications for hybrid fitness in nature.

A sensory bias overrides learned preferences of bumblebees for honest signals in Mimulus guttatus

Insect pollinators readily learn olfactory cues, and this is expected to select for ‘honest signals' that provide reliable information about floral rewards. However, plants might alternatively produce signals that exploit pollinators' sensory biases, thereby relaxing selection for signal honesty. We examined the innate and learned preferences of Bombus impatiens for Mimulus guttatus floral scent phenotypes corresponding to different levels of pollen rewards in the presence and absence of the innately attractive floral volatile compound β-trans-bergamotene. Bees learned to prefer honest signals after foraging on live M. guttatus flowers, but only exhibited this preference when presented floral scent phenotypes that did not include β-trans-bergamotene. Our results suggest that a sensory bias for β-trans-bergamotene overrides the ability of B. impatiens to use honest signals when foraging on M. guttatus . This may represent a deceptive pollination strategy that allows plants to minimize investment in costly rewards without incurring reduced rates of pollinator visitation.

Population genomic and historical analysis suggests a global invasion by bridgehead processes in Mimulus guttatus

Imperfect historical records and complex demographic histories present challenges for reconstructing the history of biological invasions. Here, we combine historical records, extensive worldwide and genome-wide sampling, and demographic analyses to investigate the global invasion of Mimulus guttatus from North America to Europe and the Southwest Pacific. By sampling 521 plants from 158 native and introduced populations genotyped at >44,000 loci, we determined that invasive M. guttatus was first likely introduced to the British Isles from the Aleutian Islands (Alaska), followed by admixture from multiple parts of the native range. We hypothesise that populations in the British Isles then served as a bridgehead for vanguard invasions worldwide. Our results emphasise the highly admixed nature of introduced M. guttatus and demonstrate the potential of introduced populations to serve as sources of secondary admixture, producing novel hybrids. Unravelling the history of biological invasions provides a starting point to understand how invasive populations adapt to novel environments.

Divergence in bidirectional plant-soil feedbacks between montane annual and coastal perennial ecotypes of yellow monkeyflower (Mimulus guttatus)

SUMMARYUnderstanding the physiological and genetic mechanisms underlying plant variation in interactions with root-associated biota (RAB) requires a micro-evolutionary approach. We use locally adapted montane annual and coastal perennial ecotypes of Mimulus guttatus (yellow monkeyflower) to examine population-scale differences in plant-RAB-soil feedbacks.We characterized fungal communities for the two ecotypes in-situ and used a full-factorial greenhouse experiment to investigate the effects of plant ecotype, RAB source, and soil origin on plant performance and endophytic root fungal communities.The two ecotypes harbored different fungal communities and responsiveness to soil biota was highly context-dependent. Soil origin, RAB source, and plant ecotype all affected the intensity of biotic feedbacks on plant performance. Feedbacks were primarily negative, and we saw little evidence of local adaptation to either soils or RAB. Both RAB source and soil origin significantly shaped fungal communities in roots of experimental plants. Further, the perennial ecotype was more colonized by arbuscular mycorrhizal fungi (AMF) than the montane ecotype, and preferentially recruited home AMF taxa.Our results suggest life history divergence and distinct edaphic habitats shape plant responsiveness to RAB and influence specific associations with potentially mutualistic root endophytic fungi. Our results advance the mechanistic study of intraspecific variation in plant–soil–RAB interactions.