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1. The genetics of extreme microgeographic adaptation: an integrated approach identifies a major gene underlying leaf trichome divergence in Yellowstone Mimulus guttatus

   https://doi.org/10.1111/mec.13753  

   Hendrick, Margaret F. ; Finseth, Findley R. ; Mathiasson, Minna E. ; Palmer, Kristen A. ; Broder, Emma M. ; Breigenzer, Peter ; Fishman, Lila ( August 2016 , Molecular Ecology)

   Microgeographic adaptation provides a particularly interesting context for understanding the genetic basis of phenotypic divergence and may also present unique empirical challenges. In particular, plant adaptation to extreme soil mosaics may generate barriers to gene flow or shifts in mating system that confound simple genomic scans for adaptive loci. Here, we combine three approaches – quantitative trait locus (QTL) mapping of candidate intervals in controlled crosses, population resequencing (PoolSeq) and analyses of wild recombinant individuals – to investigate one trait associated withMimulus guttatus(yellow monkeyflower) adaptation to geothermal soils in Yellowstone National Park. We mapped a majorQTLcausing dense leaf trichomes in thermally adapted plants to a <50‐kb region of linkage Group 14 (Tr14) previously implicated in trichome divergence between independentM. guttatuspopulations. A PoolSeq scan of Tr14 region revealed a cluster of six genes, coincident with the inferredQTLpeak, with high allele frequency differences sufficient to explain observed phenotypic differentiation. One of these, the R2R3MYBtranscription factor Migut.N02661, is a plausible functional candidate and was also strongly associated (r² = 0.27) with trichome phenotype in analyses of wild‐collected admixed individuals. Although functional analyses will be necessary to definitively link molecular variants in Tr14 with trichome divergence, our analyses are a major step in that direction. They point to a simple, and parallel, genetic basis for one axis ofMimulus guttatusadaptation to an extreme habitat, suggest a broadly conserved genetic basis for trichome variation across flowering plants and pave the way for further investigations of this challenging case of microgeographic incipient speciation.

    

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

   https://doi.org/10.1093/genetics/iyab189  

   Brown, Keely E. ; Kelly, John K. ; Wright, ed., S. ( November 2021 , Genetics)

   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 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 superabundance 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 coexpressed 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.

    

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3. Museum Genomics of an Agricultural Super-Pest, the Colorado Potato Beetle, Leptinotarsa decemlineata (Chrysomelidae), Provides Evidence of Adaptation from Standing Variation

   https://doi.org/10.1093/icb/icac137  

   Cohen, Zachary P. ; François, Olivier ; Schoville, Sean D. ( August 2022 , Integrative and Comparative Biology)

   Despite extensive research on agricultural pests, our knowledge about their evolutionary history is often limited. A mechanistic understanding of the demographic changes and modes of adaptation remains an important goal, as it improves our understanding of organismal responses to environmental change and our ability to sustainably manage pest populations. Emerging genomic datasets now allow for characterization of demographic and adaptive processes, but face limits when they are drawn from contemporary samples, especially in the context of strong demographic change, repeated selection, or adaptation involving modest shifts in allele frequency at many loci. Temporal sampling, however, can improve our ability to reconstruct evolutionary events. Here, we leverage museum samples to examine whether population genomic diversity and structure has changed over time, and to identify genomic regions that appear to be under selection. We focus on the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say 1824; Coleoptera: Chrysomelidae), which is widely regarded as a super-pest due to its rapid, and repeated, evolution to insecticides. By combining whole genome resequencing data from 78 museum samples with modern sampling, we demonstrate that CPB expanded rapidly in the 19th century, leading to a reduction in diversity and limited genetic structure from the Midwest to Northeast United States. Temporal genome scans provide extensive evidence for selection acting in resistant field populations in Wisconsin and New York, including numerous known insecticide resistance genes. We also validate these results by showing that known selective sweeps in modern populations are identified by our genome scan. Perhaps most importantly, temporal analysis indicates selection on standing genetic variation, as we find evidence for parallel evolution in the two geographical regions. Parallel evolution involves a range of phenotypic traits not previously identified as under selection in CPB, such as reproductive and morphological functional pathways that might be important for adaptation to agricultural habitats.

    

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4. Gene regulation and speciation in a migratory divide between songbirds

   https://doi.org/10.1038/s41467-023-44352-2  

   Louder, Matthew I. M. ; Justen, Hannah ; Kimmitt, Abigail A. ; Lawley, Koedi S. ; Turner, Leslie M. ; Dickman, J. David ; Delmore, Kira E. ( January 2024 , Nature Communications)

   Behavioral variation abounds in nature. This variation is important for adaptation and speciation, but its molecular basis remains elusive. Here, we use a hybrid zone between two subspecies of songbirds that differ in migration – an ecologically important and taxonomically widespread behavior---to gain insight into this topic. We measure gene expression in five brain regions. Differential expression between migratory states was dominated by circadian genes in all brain regions. The remaining patterns were largely brain-region specific. For example, expression differences between the subspecies that interact with migratory state likely help maintain reproductive isolation in this system and were documented in only three brain regions. Contrary to existing work on regulatory mechanisms underlying species-specific traits, two lines of evidence suggest that trans- (vs. cis) regulatory changes underlie these patterns – no evidence for allele-specific expression in hybrids and minimal associations between genomic differentiation and expression differences. Additional work with hybrids shows expression levels were often distinct (transgressive) from parental forms. Behavioral contrasts and functional enrichment analyses allowed us to connect these patterns to mitonuclear incompatibilities and compensatory responses to stress that could exacerbate selection on hybrids and contribute to speciation.

    

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5. An updated gene atlas for maize reveals organ‐specific and stress‐induced genes

   https://doi.org/10.1111/tpj.14184  

   Hoopes, Genevieve M. ; Hamilton, John P. ; Wood, Joshua C. ; Esteban, Eddi ; Pasha, Asher ; Vaillancourt, Brieanne ; Provart, Nicholas J. ; Buell, C. Robin ( January 2019 , The Plant Journal)

   Maize (Zea maysL.), a model species for genetic studies, is one of the two most important crop species worldwide. The genome sequence of the reference genotype, B73, representative of the stiff stalk heterotic group was recently updated (AGPv4) using long‐read sequencing and optical mapping technology. To facilitate the use ofAGPv4 and to enable functional genomic studies and association of genotype with phenotype, we determined expression abundances for replicatedmRNA‐sequencing datasets from 79 tissues and five abiotic/biotic stress treatments revealing 36 207 expressed genes. Characterization of the B73 transcriptome across six organs revealed 4154 organ‐specific and 7704 differentially expressed (DE) genes following stress treatment. Gene co‐expression network analyses revealed 12 modules associated with distinct biological processes containing 13 590 genes providing a resource for further association of gene function based on co‐expression patterns. Presence−absence variants (PAVs) previously identified using whole genome resequencing data from 61 additional inbred lines were enriched in organ‐specific and stress‐induced DE genes suggesting thatPAVs may function in phenological variation and adaptation to environment. Relative to core genes conserved across the 62 profiled inbreds,PAVs have lower expression abundances which are correlated with their frequency of dispersion across inbreds and on average have significantly fewer co‐expression network connections suggesting that a subset ofPAVs may be on an evolutionary path to pseudogenization. To facilitate use by the community, we developed the Maize Genomics Resource website (maize.plantbiology.msu.edu) for viewing and data‐mining these resources and deployed two new views on the maize electronic Fluorescent Pictograph Browser (bar.utoronto.ca/efp_maize).

    

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