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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. Reproductive isolation and introgression between sympatric Mimulus species

   https://doi.org/10.1111/mec.13630  

   Kenney, Amanda M. ; Sweigart, Andrea L. ( May 2016 , Molecular Ecology)

   Incompletely isolated species provide an opportunity to investigate the genetic mechanisms and evolutionary forces that maintain distinct species in the face of ongoing gene flow. Here, we use field surveys and reduced representation sequencing to characterize the patterns of reproductive isolation, admixture and genomic divergence between populations of the outcrossing wildflowerMimulus guttatusand selfingM. nasutus. Focusing on a single site where these two species have come into secondary contact, we find that phenological isolation is strong, although incomplete, and is likely driven by divergence in response to photoperiod. In contrast to previous field studies, which have suggested that F₁‐hybrid formation might be rare, we discover patterns of genomic variation consistent with ongoing introgression. Strikingly, admixed individuals vary continuously from highly admixed to nearly pureM. guttatus, demonstrating ongoing hybridization and asymmetric introgression fromM. nasutusintoM. guttatus. Patterns of admixture and divergence across the genome show that levels of introgression are more variable than expected by chance. Some genomic regions show a reduced introgression, including one region that overlaps a critical photoperiodQTL, whereas other regions show elevated levels of interspecific gene flow. In addition, we observe a genome‐wide negative relationship between absolute divergence and the local recombination rate, potentially indicating natural selection againstM. nasutusancestry inM. guttatusgenetic backgrounds. Together, our results suggest thatMimulusspeciation is both ongoing and dynamic and that a combination of divergence in phenology and mating system, as well as selection against interspecific alleles, likely maintains these sympatric species.

    

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3. Genomic evidence for convergent evolution of a key trait underlying divergence in island birds

   https://doi.org/10.1111/mec.14116  

   Cooper, Elizabeth A. ; Uy, J. Albert C. ( April 2017 , Molecular Ecology)

   Reproductive isolation can be initiated by changes in one or a few key traits that prevent random mating among individuals in a population. During the early stages of speciation, when isolation is often incomplete, there will be a heterogeneous pattern of differentiation across regions of the genome between diverging populations, with loci controlling these key traits appearing the most distinct as a result of strong diversifying selection. In this study, we used Illumina‐sequenced ddRADtags to identify genomewide patterns of differentiation in three recently diverged island populations of theMonarcha castaneiventrisflycatcher of the Solomon Islands. Populations of this species have diverged in plumage colour, and these differences in plumage colour, in turn, are used in conspecific recognition and likely important in reproductive isolation. Previous candidate gene sequencing identified point mutations inMC1RandASIP, both known pigmentation genes, to be associated with the difference in plumage colour between islands. Here, we show that background levels of genomic differentiation based on over 70,000SNPs are extremely low between populations of distinct plumage colour, with no loci reaching the level of differentiation found in either candidate gene. Further, we found that a phylogenetic analysis based on theseSNPs produced a taxonomy wherein the two melanic populations appear to have evolved convergently, rather than from a single common ancestor, in contrast to their original classification as a single subspecies. Finally, we found evidence that the pattern of low genomic differentiation is the result of both incomplete lineage sorting and gene flow between populations.

    

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4. Ecological genomics of local adaptation in Cornus florida L. by genotyping by sequencing

   https://doi.org/10.1002/ece3.2623  

   Pais, Andrew L. ; Whetten, Ross W. ; Xiang, Qiu‐Yun ( December 2016 , Ecology and Evolution)

   Discovering local adaptation, its genetic underpinnings, and environmental drivers is important for conserving forest species. Ecological genomic approaches coupled with next‐generation sequencing are useful means to detect local adaptation and uncover its underlying genetic basis in nonmodel species. We report results from a study on flowering dogwood trees (Cornus florida L.) using genotyping by sequencing (GBS). This species is ecologically important to easternUSforests but is severely threatened by fungal diseases. We analyzed subpopulations in divergent ecological habitats within North Carolina to uncover loci under local selection and associated with environmental–functional traits or disease infection. At this scale, we tested the effect of incorporating additional sequencing before scaling for a broader examination of the entire range. To test for biases ofGBS, we sequenced two similarly sampled libraries independently from six populations of three ecological habitats. We obtained environmental–functional traits for each subpopulation to identify associations with genotypes via latent factor mixed modeling (LFMM) and gradient forests analysis. To test whether heterogeneity of abiotic pressures resulted in genetic differentiation indicative of local adaptation, we evaluatedF_stper locus while accounting for genetic differentiation between coastal subpopulations and Piedmont‐Mountain subpopulations. Of the 54 candidate loci with sufficient evidence of being under selection among both libraries, 28–39 were Arlequin–BayeScanF_stoutliers. ForLFMM, 45 candidates were associated with climate (of 54), 30 were associated with soil properties, and four were associated with plant health. Reanalysis of combined libraries showed that 42 candidate loci still showed evidence of being under selection. We conclude environment‐driven selection on specific loci has resulted in local adaptation in response to potassium deficiencies, temperature, precipitation, and (to a marginal extent) disease. High allele turnover along ecological gradients further supports the adaptive significance of loci speculated to be under selection.

    

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5. Genetic architecture, biochemical underpinnings and ecological impact of floral UV patterning

   https://doi.org/10.1111/mec.13542  

   Brock, Marcus T. ; Lucas, Lauren K. ; Anderson, Nickolas A. ; Rubin, Matthew J. ; Cody Markelz, R. J. ; Covington, Michael F. ; Devisetty, Upendra K. ; Chapple, Clint ; Maloof, Julin N. ; Weinig, Cynthia ( February 2016 , Molecular Ecology)

   Floral attraction traits can significantly affect pollinator visitation patterns, but adaptive evolution of these traits may be constrained by correlations with other traits. In some cases, molecular pathways contributing to floral attraction are well characterized, offering the opportunity to explore loci potentially underlying variation among individuals. Here, we quantify the range of variation in floralUVpatterning (i.e.UV‘bulls‐eye nectar guides) among crop and wild accessions ofBrassica rapa. We then use experimental crosses to examine the genetic architecture, candidate loci and biochemical underpinnings of this patterning as well as phenotypic manipulations to test the ecological impact. We find qualitative variation inUVpatterning between wild (commonly lackingUVpatterns) and crop (commonly exhibitingUVpatterns) accessions. Similar to the majority of crops, recombinant inbred lines (RILs) derived from an oilseed crop × WIfast‐plant^®cross exhibitUVpatterns, the size of which varies extensively among genotypes. InRILs, we further observe strong statistical‐genetic andQTLcorrelations within petal morphological traits and within measurements of petalUVpatterning; however, correlations between morphology andUVpatterning are weak or nonsignificant, suggesting thatUVpatterning is regulated and may evolve independently of overall petal size.HPLCanalyses reveal a high concentration of sinapoyl glucose inUV‐absorbing petal regions, which, in concert with physical locations ofUV‐traitQTLs, suggest a regulatory and structural gene as candidates underlying observed quantitative variation. Finally, insects prefer flowers withUVbulls‐eye patterns over those that lack patterns, validating the importance ofUVpatterning in pollen‐limited populations ofB. rapa.

    

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