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Andrew, Rose L.; Rieseberg, Loren H. 2013-03-07 Early in speciation, when populations are undergoing the transition from local adaptation to incipient species, is when a number of transient, but potentially important, processes appear to be most easily detected. These include signatures of selective sweeps that can point to asymmetry in selection between habitats, divergence hitchhiking and associations of adaptive genes with environments. In a genomic comparison of ecotypes of the prairie sunflower, Helianthus petiolaris, occurring at Great Sand Dunes National Park (Colorado), we found that selective sweeps were mainly restricted to the dune ecotype and that there was variation across the genome in whether proximity to the non-dune population constrained or promoted divergence. The major regions of divergence were few and large between ecotypes, in contrast with an interspecific comparison between H. petiolaris and a sympatric congener, H. annuus. In general, the large regions of divergence observed in the ecotypic comparison swamped locus-specific associations with environmental variables. In both comparisons, regions of high divergence occurred in portions of the genetic map with high marker density, probably reflecting regions of low recombination. The difference in genomic distributions of highly divergent regions between ecotypic and interspecific comparisons highlights the value of studies spanning the spectrum of speciation in related taxa.
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Baute, Gregory J.; Kane, Nolan C.; Grassa, Christopher J.; Lai, Zhao; Rieseberg, Loren H. 2015-12-02 • The development of modern crops typically involves both selection and hybridization, but to date most studies have focused on the former. In the present study we explore how both processes, and their interactions, have molded the genome of the cultivated sunflower, a globally important oilseed. • To identify genes targeted by selection during the domestication and improvement of sunflower, and to detect post-domestication hybridization with wild species, we analyzed transcriptome sequences of 80 genotypes, including wild, landrace, and modern lines of Helianthus annuus, as well as two cross-compatible wild relatives, H. argophyllus and H. petiolaris. • Outlier analyses identified 122 and 15 candidate genes associated with domestication and improvement, respectively. As in several previous studies, genes putatively involved in oil biosynthesis were the most extreme outliers. Additionally, several promising associations were observed with previously mapped QTLs, such as branching. Admixture analyses revealed that all of the modern cultivar genomes we examined contained one or more introgressions from wild populations, with every chromosome having evidence of introgression in at least one modern line. • Cumulatively, introgressions cover approximately 10% of the cultivated sunflower genome. Surprisingly, introgressions do not avoid candidate domestication genes likely because of the re-introduction of branching.
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Moyers, Brook T.; Rieseberg, Loren H. 2016-06-13 Substantial intraspecific variation in life history is rare and potentially a signal of incipient ecological speciation, if variation is driven by geographically heterogenous natural selection. We present the first report of extensive life history polymorphism in Helianthus argophyllus, the silverleaf sunflower, and examine evidence for its evolution by divergent selection. In 18 populations sampled from across the species range and grown in a common garden, most quantitative traits covaried such that individuals could be assigned to two distinct life history syndromes: tall and late flowering with small initial flowerheads, or short and early flowering with larger initial flowerheads. Helianthus argophyllus exhibits regional genetic structure, but this population structure does not closely correspond with patterns of phenotypic variation. The early-flowering syndrome is primarily observed in populations from coastal barrier islands, while populations from the nearby mainland coast, although geographically and genetically close, are primarily late flowering. Additionally, several traits are more differentiated among regions than expected based on neutral genetic divergence (QST > FST), including the first principal component score corresponding with life history syndrome. This discordance between patterns of phenotypic and genetic variation suggests that divergent selection is driving genetic differences in life history across the species range. If so, the silverleaf sunflower may be in early stages of ecological speciation.
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Thompson, Kenneth; Urquhart-Cronish, Mackenzie; Whitney, Kenneth D.; Rieseberg, Loren H.; Schluter, Dolph 2020-11-12 <p>Compared to those of their parents, are the traits of first-generation (F<sub>1</sub>) hybrids typically intermediate, biased toward one parent, or mismatched for alternative parental phenotypes? And how does hybrid trait expression affect fitness? To address this empirical gap, we compiled data from 198 studies in which traits were measured in a common environment for two parent taxa and their F<sub>1</sub> hybrids. We find that individual traits in F<sub>1</sub>s are, on average, halfway between the parental midpoint and one parental value (e.g., hybrid trait values are 0.75 if parents'values are 0 &amp;1). When considering pairs of traits together, a hybrid's bivariate phenotype tends to resemble one parent (pairwise parent-bias) about 50 % more than the other while also exhibiting a similar magnitude of mismatch due to different traits having dominance in conflicting directions. We detect no phylogenetic signal nor an effect of parental genetic distance on dominance or mismatch. Using data from an experimental field planting of recombinant hybrid sunflowers, we illustrate that pairwise parent-bias improves fitness whereas pairwise mismatch reduces fitness. In sum, our study has three major conclusions. First, hybrids between ecologically divergent natural populations are not phenotypically intermediate but rather exhibit substantial mismatch while also resembling one parent more than the other. Second, dominance and mismatch do not seem to be governed by general rules but rather by the idiosyncratic evolutionary trajectories of individual traits in individual populations or species. Finally, selection against hybrids likely results from selection against both intermediate and mismatched phenotypes.</p>
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Andrew, Rose L.; Ostevik, Katherine L.; Ebert, Daniel P.; Rieseberg, Loren H. 2011-12-14 Isolation by adaptation increases divergence at neutral loci when natural selection against immigrants reduces the rate of gene flow between different habitats. This can occur early in the process of adaptive divergence and is a key feature of ecological speciation. Despite the ability of isolation by distance and other forms of landscape resistance to produce similar patterns of neutral divergence within species, few studies have used landscape genetics to control for these other forces. We have studied the divergence of Helianthus petiolaris ecotypes living in active sand dunes and adjacent non-dune habitat, using landscape genetics approaches, such as circuit theory and multiple regression of distance matrices, in addition to coalescent modelling. Divergence between habitats was significant, but not strong, and was shaped by isolation by distance. We expected that increased resistance due to patchy and unfavourable habitat in the dunes would contribute to divergence. Instead, we found that landscape resistance models with lower resistance in the dunes performed well as predictors of genetic distances among subpopulations. Nevertheless, habitat class remained a strong predictor of genetic distance when controlling for isolation by resistance and isolation by distance. We also measured environmental variables at each site and confirmed that specific variables, especially soil nitrogen and vegetation cover, explained a greater proportion of variance in genetic distance than did landscape or the habitat classification alone. Asymmetry in effective population sizes and numbers of migrants per generation was detected using coalescent modelling with Bayesian inference, which is consistent with incipient ecological speciation being driven by the dune habitat.
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Turner, Kathryn G.; Fréville, Hélène; Rieseberg, Loren H. 2016-06-18 Phenotypic differentiation in size and fecundity between native and invasive populations of a species has been suggested as a causal driver of invasion in plants. Local adaptation to novel environmental conditions through a micro-evolutionary response to natural selection may lead to phenotypic differentiation and fitness advantages in the invaded range. Local adaptation may occur along a stress tolerance trade-off, favoring individuals that, in benign conditions, shift resource allocation from stress tolerance to increased vigor and fecundity and, therefore, invasiveness. Alternately, the typically disturbed invaded range may select for a plastic, generalist strategy, making phenotypic plasticity the main driver of invasion success. To distinguish between these hypotheses, we performed a field common garden and tested for genetically based phenotypic differentiation, resource allocation shifts in response to water limitation, and local adaptation to the environmental gradient which describes the source locations for native and invasive populations of diffuse knapweed (Centaurea diffusa). Plants were grown in an experimental field in France (naturalized range) under water addition and limitation conditions. After accounting for phenotypic variation arising from environmental differences among collection locations, we found evidence of genetic variation between the invasive and native populations for most morphological and life-history traits under study. Invasive C. diffusa populations produced larger, later maturing, and therefore potentially fitter individuals than native populations. Evidence for local adaptation along a resource allocation trade-off for water limitation tolerance is equivocal. However, native populations do show evidence of local adaptation to an environmental gradient, a relationship which is typically not observed in the invaded range. Broader analysis of the climatic niche inhabited by the species in both ranges suggests that the physiological tolerances of C. diffusa may have expanded in the invaded range. This observation could be due to selection for plastic, “general-purpose” genotypes with broad environmental tolerances. https://creativecommons.org/publicdomain/zero/1.0/
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Yeaman, Sam; Hodgins, Kathryn A.; Suren, Haktan; Nurkowski, Kristin A.; Holliday, Jason A.; Rieseberg, Loren H.; Aitken, Sally N. 2015-03-19 Species respond to environmental stress through a combination of genetic adaptation and phenotypic plasticity, both of which may be important for survival in the face of climatic change. By characterizing the molecular basis of plastic responses and comparing patterns among species, it is possible to identify how such traits evolve. Here, we use de novo transcriptome assembly and RNA-seq to explore how patterns of gene expression differ in response to temperature, moisture, and light regime treatments in lodgepole pine (Pinus contorta) and interior spruce (a natural hybrid population of Picea glauca and Picea engelmannii). We found wide evidence for an effect of treatment on expression within each species, with 6,413 and 11,658 differentially expressed genes identified in spruce and pine, respectively. Comparing patterns of expression among these species, we found that 74% of all orthologs with differential expression had a pattern that was conserved in both species, despite 140 million years of evolution. We also found that the specific treatments driving expression patterns differed between genes with conserved vs. diverged patterns of expression. We conclude that natural selection has likely played a role in shaping plastic responses to environment in these species.
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Yeaman, Sam; Hodgins, Kathryn A.; Lotterhos, Katie E.; Suren, Haktan; Nadeau, Simon; Nurkowski, Kristin A.; Smets, Pia; Wang, Tongli; Gray, Laura K.; Liepe, Katharina J.; Hamann, Andreas; Holliday, Jason A.; Whitlock, Michael C.; Rieseberg, Loren H.; Aitken, Sally N. 2016-09-30 When confronted with an adaptive challenge, such as extreme temperature, closely related species frequently evolve similar phenotypes using the same genes. Although such repeated evolution is thought to be less likely in highly polygenic traits and distantly related species, this has not been tested at the genome scale. We performed a population genomic study of convergent local adaptation among two distantly related species, lodgepole pine and interior spruce. We identified a suite of 47 genes, enriched for duplicated genes, with variants associated with spatial variation in temperature or cold hardiness in both species, providing evidence of convergent local adaptation despite 140 million years of separate evolution. These results show that adaptation to climate can be genetically constrained, with certain key genes playing nonredundant roles.
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Hahn, Min A.; Rieseberg, Loren H. 2016-11-03 Biological invasions are often associated with multiple introductions and genetic admixture of previously isolated populations. In addition to enhanced evolutionary potential through increased genetic variation, admixed genotypes may benefit from heterosis, which could contribute to their increased performance and invasiveness. To deepen our understanding of the mechanisms and management strategies for biological invasions, we experimentally studied whether intraspecific admixture causes heterosis in common ragweed (Ambrosia artemisiifolia) by comparing the performance of crosses (F1) between populations relative to crosses within these populations for each range (native, introduced) under different ecologically relevant conditions (control, drought, competition, simulated herbivory). Performance of admixed genotypes was highly variable, ranging from strong heterotic effects to weak outbreeding depression. Moreover, heterosis was not uniformly observed among between-population crosses, but certain native population crosses showed considerable heterosis, especially under simulated herbivory. In contrast, heterosis was largely absent in crosses from the introduced range, possibly implying that these populations were already admixed and benefit little from further mixing. In conclusion, these results support the hypothesis that heterosis may contribute to biological invasions, and indicate the need to minimize new introductions of exotic species, even if they are already present in the introduced range.
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Rieseberg, Loren H.; Andrew, Rose L.; Kane, Nolan C.; Baute, Greg J.; Grassa, Christopher J. 2012-09-17 The genomics of local adaptation is an increasingly active field, providing insights into the forces driving ecological speciation and the repeatability of evolution. Demography and gene flow play an important role in determining the paths by which parallel evolution occurs and the genomic signatures of adaptation. In the annual sunflowers, hybridization between species has repeatedly led to the colonization of extreme habitats, such as sand dunes. In a new case of adaptation to sand dunes that occurs in populations of H. petiolaris growing at Great Sand Dunes National Park and Preserve (Colorado), we wished to determine the age and long-term migration patterns of the system, as well as its ancestry. We addressed these questions with restriction-associated DNA (RAD) sequence data, aligned to a reference transcriptome. In an isolation with migration model using RAD sequences, coalescent analysis showed that the dune ecotype originated since the last ice age, which is very recent compared with the hybrid dune species, H. anomalus. Large effective population sizes and substantial numbers of gene migrants per generation between dune and nondune ecotypes explained the highly heterogeneous divergence observed among loci. Analysis of RAD-derived SNPs identified heterogeneous divergence between the dune and nondune ecotypes, as well as identifying its nearest relative. Our results did not support the hypothesis that the dune ecotype has hybrid ancestry, suggesting that adaptation of sunflowers to dunes has occurred by multiple mechanisms. The ancestry and long-term history of gene flow between incipient sunflower species provides valuable context for our understanding of ecological speciation and parallel adaptation.
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Renaut, Sebastien; Owens, Gregory L.; Rieseberg, Loren H. 2013-11-26 The repeated evolution of traits in organisms facing similar environmental conditions is considered to be fundamental evidence for the role of natural selection in moulding phenotypes. Yet, aside from case studies of parallel evolution and its genetic basis, the repeatability of evolution at the level of the whole genome remains poorly characterized. Here, through the use of transcriptome sequencing, we examined genomic divergence for three pairs of sister species of sunflowers. Two of the pairs (Helianthus petiolaris – H. debilis and H. annuus – H. argophyllus) have diverged along a similar latitudinal gradient and presumably experienced similar selective pressure. In contrast, a third species pair (H. exilis – H. bolanderi) diverged along a longitudinal gradient. Analyses of divergence, as measured in terms of FST, indicated little repeatability across the three pairs of species for individual genetic markers (SNPs), modest repeatability at the level of individual genes and the highest repeatability when large regions of the genome were compared. As expected, higher repeatability was observed for the two species pairs that have diverged along a similar latitudinal gradient, with genes involved in flowering time among the most divergent genes. Genes showing extreme low or high differentiation were more similar than genes showing medium levels of divergence, implying that both purifying and divergent selection contributed to repeatable patterns of divergence. The location of a gene along the chromosome also predicted divergence levels, presumably because of shared heterogeneity in both recombination and mutation rates. In conclusion, repeated genome evolution appeared to result from both similar selective pressures and shared local genomic landscapes.
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Renaut, Sebastien; Rieseberg, Loren H. 2016-04-29 For populations to maintain optimal fitness, harmful mutations must be efficiently purged from the genome. Yet, under circumstances that diminish the effectiveness of natural selection, such as the process of plant and animal domestication, deleterious mutations are predicted to accumulate. Here, we compared the load of deleterious mutations in 21 accessions from natural populations and 19 domesticated accessions of the common sunflower using whole-transcriptome single nucleotide polymorphism data. Although we find that genetic diversity has been greatly reduced during domestication, the remaining mutations were disproportionally biased toward nonsynonymous substitutions. Bioinformatically predicted deleterious mutations affecting protein function were especially strongly over-represented. We also identify similar patterns in two other domesticated species of the sunflower family (globe artichoke and cardoon), indicating that this phenomenon is not due to idiosyncrasies of sunflower domestication or the sunflower genome. Finally, we provide unequivocal evidence that deleterious mutations accumulate in low recombining regions of the genome, due to the reduced efficacy of purifying selection. These results represent a conundrum for crop improvement efforts. Although the elimination of harmful mutations should be a long-term goal of plant and animal breeding programs, it will be difficult to weed them out because of limited recombination.
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Dempewolf, Hannes; Tesfaye, Misteru; Teshome, Abel; Bjorkman, Anne; Andrew, Rose L.; Scascitelli, Moira; Black, Scott; Bekele, Endashaw; Engels, Johannes M. M.; Cronk, Quentin C. B.; Rieseberg, Loren H.; Bjorkman, Anne D. 2015-02-26 Noug (Guizotia abyssinica) is a semi-domesticated oil-seed crop, which is primarily cultivated in Ethiopia. Unlike its closest crop relative, sunflower, noug has small seeds, small flowering heads, many branches, many flowering heads, indeterminate flowering, and it shatters in the field. Here we conducted common garden studies and microsatellite analyses of genetic variation to test whether high levels of crop-wild gene flow and/or unfavorable phenotypic correlations have hindered noug domestication. With the exception of one population, analyses of microsatellite variation failed to detect substantial recent admixture between noug and its wild progenitor. Likewise, only very weak correlations were found between seed mass and the number or size of flowering heads. Thus, noug's ‘atypical’ domestication syndrome does not seem to be a consequence of recent introgression or unfavorable phenotypic correlations. Nonetheless, our data do reveal evidence of local adaptation of noug cultivars to different precipitation regimes, as well as high levels of phenotypic plasticity, which may permit reasonable yields under diverse environmental conditions. Why noug has not been fully domesticated remains a mystery, but perhaps early farmers selected for resilience to episodic drought or untended environments rather than larger seeds. Domestication may also have been slowed by noug's outcrossing mating system.
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Bock, Dan G.; Kantar, Michael B.; Caseys, Celine; Matthey-Doret, Remi; Rieseberg, Loren H. 2019-03-16 Invasion success of species introduced to novel environments may be facilitated by adaptive evolution and by phenotypic plasticity. Here we investigate the independent and joint contribution of both mechanisms as drivers of invasiveness in the perennial sunflower Helianthus tuberosus. We show that invasive genotypes have multiple origins, and that invasive spread was facilitated by the repeated evolution of extreme values in a single trait, clonality. In line with genetic accommodation theory, we establish that this evolutionary transition occurred by refining a preexisting plastic response of clonality to water availability. Further, we demonstrate that under the non-drought conditions typically experienced by this plant in its introduced range, invasive spread is mediated by hybrid vigor and/or two major additive-effect loci, and that these mechanisms are complementary. Thus, in H. tuberosus, evolution of invasiveness was facilitated by phenotypic plasticity, and involved the use of multiple genetic solutions to achieve the same invasiveness trait.
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Hodgins, Kathryn A.; Lai, Zhao; Oliveira, Luiz O.; Still, David W.; Scascitelli, Moira; Barker, Michael S.; Kane, Nolan C.; Dempewolf, Hannes; Kozik, Alex; Kesseli, Richard V.; Burke, John M.; Michelmore, Richard W.; Rieseberg, Loren H. 2013-08-19 Although the Compositae harbours only two major food crops, sunflower and lettuce, many other species in this family are utilized by humans and have experienced various levels of domestication. Here we have used next generation sequencing technology to develop 15 reference transcriptome assemblies for Compositae crops or their wild relatives. These data allow us to gain insight into the evolutionary and genomic consequences of plant domestication. Specifically, we performed Illumina sequencing of Cichorium endivia, Cichorium intybus, Echinacea angustifolia, Iva annua, Helianthus tuberosus, Dahlia hybrida, Leontodon taraxacoides and Glebionis segetum, as well 454 sequencing of Guizotia scabra, Stevia rebaudiana, Parthenium argentatum and Smallanthus sonchifolius. Illumina reads were assembled using Trinity, and 454 reads were assembled using MIRA and CAP3. We evaluated the coverage of the transcriptomes using BLASTX analysis of a set of ultra-conserved orthologs (UCOs) and recovered most of these genes (88-98%). We found a correlation between contig length and read length for the 454 assemblies, and greater contig lengths for the 454 compared to the Illumina assemblies. This suggests that longer reads can aid in the assembly of more complete transcripts. Finally, we compared the divergence of orthologs at synonymous sites (Ks) between Compositae crops and their wild relatives and found greater divergence when the progenitors were self-incompatible. We also found greater divergence between pairs of taxa that had some evidence of post-zygotic isolation. For several more distantly related congeners, such as chicory and endive, we identified a signature of introgression in the distribution of Ks values.
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Mayrose, Itay; Zhan, Shing H.; Rothfels, Carl J.; Magnuson-Ford, Karen; Barker, Michael S.; Rieseberg, Loren H.; Otto, Sarah P. 2011-08-19 Polyploidy, the doubling of genomic content, is a widespread feature, especially among plants, yet its macro-evolutionary impacts are contentious. Traditionally, polyploidy has been considered an evolutionary dead-end, whereas recent genomic studies suggest that polyploidy has been a key driver of macro-evolutionary success. Here we examine the consequences of polyploidy on the time scale of genera across a diverse set of vascular plants, encompassing hundreds of inferred polyploidization events. Likelihood-based analyses indicate that polyploids generally exhibit lower speciation rates and higher extinction rates than diploids, providing the first quantitative corroboration of the dead-end hypothesis. The increased speciation rates of diploids can, in part, be ascribed to their capacity to speciate via polyploidy. Only particularly “fit” lineages of polyploids may persist to enjoy longer term evolutionary success.
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Zenodo
Anstett, Daniel N.; Anstett, Julia; Sheth, Seema N.; Moxley, Dylan R.; Jahani, Mojtaba; Huang, Kaichi; Todesco, Marco; Jordan, Rebecca; Lazaro-Guevara, Jose Miguel; Rieseberg, Loren H.; Angert, Amy L. 2024-10-22 Medium-sized data input for R scripts for the paper "Evolutionary rescue during extreme drought". Files are included for "baseline" (spatial) SNP tables (baseline_filtered_variants.QUAL20_MQ40_AN80_MAF0.03_DP1SD.Baypass_table), "timeseries" (temporal) SNP tables(timeseries_filtered_variants.QUAL20_MQ40_AN80_MAF0.03_DP1SD.Baypass_table), BayesFactors for all SNPs across 9 drought associated environmental variables (env__trim.tsv), and SNP-specific nucleotide diversity for 55 baseline populations (pop_baseline_.sites.pi).   Scripts that use these files are hosted at zenodo.org/records/13964969 https://creativecommons.org/licenses/by/4.0/legalcode

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