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1. Subspecies delineation amid phenotypic, geographic and genetic discordance in a songbird

   https://doi.org/10.1111/mec.14010  

   Walsh, Jennifer ; Lovette, Irby J. ; Winder, Virginia ; Elphick, Chris S. ; Olsen, Brian J. ; Shriver, Gregory ; Kovach, Adrienne I. ( February 2017 , Molecular Ecology)

   Understanding the processes that drive divergence within and among species is a long‐standing goal in evolutionary biology. Traditional approaches to assessing differentiation rely on phenotypes to identify intra‐ and interspecific variation, but many species express subtle morphological gradients in which boundaries among forms are unclear. This intraspecific variation may be driven by differential adaptation to local conditions and may thereby reflect the evolutionary potential within a species. Here, we combine genetic and morphological data to evaluate intraspecific variation within the Nelson's (Ammodramus nelsoni) and salt marsh (Ammodramus caudacutus) sparrow complex, a group with populations that span considerable geographic distributions and a habitat gradient. We evaluated genetic structure among and within five putative subspecies ofA. nelsoniandA. caudacutususing a reduced‐representation sequencing approach to generate a panel of 1929SNPs among 69 individuals. Although we detected morphological differences among some groups, individuals sorted along a continuous phenotypic gradient. In contrast, the genetic data identified three distinct clusters corresponding to populations that inhabit coastal salt marsh, interior freshwater marsh and coastal brackish–water marsh habitats. These patterns support the current species‐level recognition but do not match the subspecies‐level taxonomy within each species—a finding which may have important conservation implications. We identified loci exhibiting patterns of elevated divergence among and within these species, indicating a role for local selective pressures in driving patterns of differentiation across the complex. We conclude that this evidence for adaptive variation among subspecies warrants the consideration of evolutionary potential and genetic novelty when identifying conservation units for this group.

    

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2. 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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3. Climate variables explain neutral and adaptive variation within salmonid metapopulations: the importance of replication in landscape genetics

   https://doi.org/10.1111/mec.13517  

   Hand, Brian K. ; Muhlfeld, Clint C. ; Wade, Alisa A. ; Kovach, Ryan P. ; Whited, Diane C. ; Narum, Shawn R. ; Matala, Andrew P. ; Ackerman, Michael W. ; Garner, Brittany A. ; Kimball, John S. ; et al ( February 2016 , Molecular Ecology)

   Understanding how environmental variation influences population genetic structure is important for conservation management because it can reveal how human stressors influence population connectivity, genetic diversity and persistence. We used riverscape genetics modelling to assess whether climatic and habitat variables were related to neutral and adaptive patterns of genetic differentiation (population‐specific and pairwiseF_ST) within five metapopulations (79 populations, 4583 individuals) of steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin,USA. Using 151 putatively neutral and 29 candidate adaptiveSNPloci, we found that climate‐related variables (winter precipitation, summer maximum temperature, winter highest 5% flow events and summer mean flow) best explained neutral and adaptive patterns of genetic differentiation within metapopulations, suggesting that climatic variation likely influences both demography (neutral variation) and local adaptation (adaptive variation). However, we did not observe consistent relationships between climate variables andF_STacross all metapopulations, underscoring the need for replication when extrapolating results from one scale to another (e.g. basin‐wide to the metapopulation scale). Sensitivity analysis (leave‐one‐population‐out) revealed consistent relationships between climate variables andF_STwithinthree metapopulations; however, these patterns were not consistent in two metapopulations likely due to small sample sizes (N = 10). These results provide correlative evidence that climatic variation has shaped the genetic structure of steelhead populations and highlight the need for replication and sensitivity analyses in land and riverscape genetics.

    

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4. Epigenetic divergence as a potential first step in darter speciation

   https://doi.org/10.1111/mec.13561  

   Smith, Tracy A. ; Martin, Michael D. ; Nguyen, Michael ; Mendelson, Tamra C. ( March 2016 , Molecular Ecology)

   Recent studies show that epigenetic variation in the form ofDNAmethylation may serve as a substrate for selection. Theory suggests that heritable epigenetic marks that increase fitness should increase in frequency in a population, and these changes may result in novel morphology, behaviour, or physiology, and ultimately reproductive isolation. Therefore, epigenetic variation might provide the first substrate for selection during the course of evolutionary divergence. This hypothesis predicts that populations in the earliest stages of divergence will differentiate in their methylome prior to any genetic differentiation. While several studies have investigated natural epigenetic variation, empirical studies that test predictions about its role in speciation are surprisingly scarce. Here, we investigateDNAmethylation variation using an isoschizomeric digest method, Methyl‐Sensitive Amplified Polymorphism, across multiple stages of evolutionary divergence in natural populations of North American stream fishes. We show that epigenetic differentiation between methylomes is greater than genetic divergence among closely related populations across two river drainages. Additionally, we demonstrate that epigenetic divergence is a stronger predictor of the strength of behavioural reproductive isolation and suggest that changes in the methylome could influence the evolution of reproductive isolation between species. Our findings suggest a role for epigenetics not only in the initiation of divergence, but also in the maintenance of species boundaries over greater evolutionary timescales.

    

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5. 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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