Loren Rieseberg


Research Classification

Research Interests

invasive plants
plant evolutionary biology

Relevant Degree Programs


Research Methodology

evolutionary genomics
ecological experiments


Postdoctoral Fellows
Any time / year round

Adaptation, Speciation, Evolution of Crops and Weeds, Bioinformatics

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Graduate Student Supervision

Doctoral Student Supervision (Jan 2008 - May 2021)
The genomics of adaptation and speciation in wild sunflowers (2021)

Uncovering the genetic and evolutionary basis of adaptation and speciation is a major focus of evolutionary biology. The recent accumulation of population-scale genomic data makes it possible to identify loci underlying adaptive divergence and speciation, as well as the genomic architecture that facilitates these processes. Chromosomal inversions, a genomic rearrangement in which a segment of a chromosome is reversed end to end, have received much attention as one of the most important genomic architectures contributing to adaption and speciation. In this thesis, I used high-quality genomic data from wild sunflowers to explore the role of inversions in adaptation and speciation. I first conducted a comprehensive literature review to investigate what we have learned about the establishment and likely evolutionary role of chromosomal inversions in plants. In my second study, I made use of reduced representation sequencing data and newly developed population genomic approaches to identify seven putative chromosomal inversions that contribute to adaptive divergence of a sand dune ecotype of the prairie sunflower (Helianthus petiolaris). I further employed comparative genetic mapping to validate the inversions and identified key environmental variables significantly associated with these inversions using genome-environment association analyses. I then broadened my study to investigate the role of inversions in molecular evolution across different wild sunflowers. I showed that inversions are ideal recombination modifiers from an evolutionary standpoint because by allowing recombination among chromosomes of the same orientation but not between orientations they can facilitate adaptive divergence with gene flow, while largely averting the accumulation of deleterious mutations due to recombination suppression. Lastly, I used multiple approaches to identify loci underlying parallel ecological divergence in two dune ecotypes in H. petiolaris and found that inversions contribute disproportionately to parallel genetic evolution. Future directions include identifying genes and mutations underlying key traits associated with the inversions, examining the association of inversions with assortative mating, and exploring the roles of other structural variants in facilitating adaptation and speciation.

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The role of adaptive evolution in the success of an agricultural weed, Helianthus annuus (2018)

If a weed is defined as a plant that is “growing where it is not wanted”, then agricultural weeds, or plants that invade and persist in cultivated fields, might be the epitome of weeds. Agricultural weeds have arisen repeatedly from wild plant species, often undergoing rapid evolution to escape eradication. While agricultural weeds thus represent an attractive opportunity to study evolutionary processes operating over short timescales, the genetic basis of local adaptation and, in cases of multiple independent weed origins, the factors influencing parallel evolution, they remain understudied. For my thesis work, I asked whether populations of common sunflower (Helianthus annuus) growing as agricultural weeds have adapted to the unique challenges posed by cultivated fields. In a common garden, I compared paired weedy and wild (i.e., non-agricultural) populations, collected over a latitudinal transect from Canada to Kansas, USA. Weedy populations grew faster and flowered earlier than wild populations, suggesting an evolutionary shift in life history strategy to prioritize growth and reproduction. One wild population from a wetland site showed the same pattern, indicating that wild sunflowers may face similar selection pressures in certain contexts. I then used whole genome resequencing to investigate the extent of parallel genetic differentiation between weedy and wild populations. Using two different metrics, a “cluster separation score” based on genetic distance matrices and FST, I identified a list of 148 differentiated genomic regions, though our analysis lacked power to distinguish true positives after correction for multiple testing, and therefore these regions are only suggestively linked to adaptation to the agricultural environment. Genes overlapping these regions were varied and included those involved in plant stress responses, flowering time genes and transporter genes linked to herbicide resistance. To connect phenotype to genotype, I conducted a genome-wide association analysis of glyphosate resistance, a trait likely critical for the success of weedy populations. At a glyphosate application rate of 0.5 kg a.e. ha-¹, or half the rate typically applied by a farmer, resistance segregated in the mapping population, with surviving plants (78.5%) showing a variety of symptoms. Mapping identified 68 SNPs suggestively associated with resistance, and three transporter proteins, among other genes.

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The genetics of contemporary evolution in an invasive perennial sunflower (2017)

While it is now widely accepted that contemporary evolution is common, we have limited information on the genetic underpinnings of these transitions. Here, I investigate this topic in invasive perennial sunflowers. First, I review the plant evolutionary biology literature to assess the validity of a common assumption, that plant organelle genome variation is selectively neutral. I show that organelle-encoded adaptations are likely, and supported both theoretically and empirically. I then rely on genome skimming to clarify the origin of Helianthus tuberosus, a hexaploid perennial sunflower and the study system I used for the rest of this thesis. Based on phylogenomic evidence, I show that H. tuberosus is an auto-allopolyploid that formed by hybridization between diploid and auto-tetraploid perennial sunflowers. This study provides an early example of the use of genome skimming for the identification of the progenitors of polyploid taxa, and facilitates studies on genome reorganization following polyploid speciation. Finally, I investigate the genetic architecture of invasiveness in H. tuberosus. I use genomic data to show that invasive genotypes originated repeatedly, and that most derive from hybridization between native and cultivated material. I then combine information from the greenhouse and from a replicated common garden, and show that increased clonal propagation is a major invasiveness trait in this system. I present evidence that high invasiveness in H. tuberosus can be achieved by hybridization and heterosis, or independent of hybridization, through the action of two major additive effect loci. Moreover, I find that these different genetic mechanisms can act synergistically, and that both have been exploited by widespread invasive clones. Collectively, these results show that invasiveness can be achieved via multiple genetic routes in the same system and during the same biological invasion event. These findings contribute to our understanding of the diverse genetic basis of contemporary evolutionary transitions.

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Hybridization in Helianthus: The genomic profiles of potential and confirmed sunflower hybrid species (2016)

Hybridization is an important evolutionary force that acts in both constructive and destructive ways. It can both swamp out rare species and create new ones. To better understand these effects I studied hybridization within the sunflower genus Helianthus from three angles. First, I used a rich literature of artificial crossing experiments in Helianthus and Madiinae to ask how fast reproductive isolation evolves and what features affect its accumulation. I show that hybrid sterility can evolve quickly and is faster in annuals than in perennials. I then examine a classic case of introgression involving Helianthus bolanderi. I use modern genomic tools to show that it is not of hybrid origin and likely not a separate species from its congener H. exilis. We do however find introgression with the invading species, H. annuus. In agreement with theory, we find that gene flow is mainly into the invading species. Lastly, I use transcriptomic data for three established homoploid hybrid species, H. anomalus, H. deserticola, and H. paradoxus, and their parents H. annuus and H. petiolaris to map the genomic composition of hybrid species. I show that composition is even or biased towards H. petiolaris. Hybrid genomes are highly recombined but are more similar in genomic composition than expected by chance, suggesting the work of selection. Furthermore, although analyses of genetic distance between the hybrid species and their parents suggests that the hybrids are older than previously appreciated, they do not appear to be fully stabilized. Lastly two of the species, H. anomalus and H. deserticola, may share a common origin. Future directions include mapping introgression in H. annuus, and modeling parental block size to determine the number of loci and strength of selection during hybrid speciation.

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The ecology and genetics of adaptation and speciation in dune sunflowers (2016)

We can learn about the factors that promote and constrain speciation by comparing multiple instances of the evolution of reproductive isolation. It is particularly useful to compare systems with similar environmental transitions because natural selection is likely responsible for any evolutionary patterns that are consistently associated with ecological variation. In this thesis, I examine two cases of putatively similar recent or incipient ecological speciation in the sunflower genus Helianthus. In each case, the divergence observed between geographically adjacent populations is associated with adaptation to sand dunes. In my first study, I comprehensively test for reproductive isolation between dune and non-dune ecotypes of H. petiolaris. Despite their recent divergence, I find that multiple reproductive barriers separate them, including post-pollination assortative mating in the form of pollen competition. In addition, I find that a striking difference in seed size between the ecotypes is a consequence of divergent natural selection, and that it leads to strong and extrinsic reproductive isolation via selection against immigrants and hybrids. I then broaden my study to include the dune endemic, H. neglectus, which is sister to typical H. petiolaris. I look for chromosomal rearrangements between H. neglectus and H. petiolaris, and find almost as many large translocations between them as between more distantly related sunflowers. Finally, I discover that larger seeds are associated with dune environments in both systems and that the genetic basis of that phenotypic evolution is partiality repeated. Taken together, these results suggest that dune adaption within H. petiolaris and between H. petiolaris and H. neglectus has similar consequences. However, it remains to be seen whether assortative mating and chromosomal evolution are unique to the evolution of dune H. petiolaris and H. neglectus, respectively. Ultimately, understanding the similarities and differences between these systems will help answer the question - how predictable is speciation?

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Ecological genomics of invasive thistle, diffuse knapweed (2015)

Invasive species are able to move into new environments, with new abiotic conditions and biotic interactions, survive, and even dominate, often within a hundred years. Much research in invasion biology has assessed whether populations of invasive plants show phenotypic or evolved genetic differences in growth and reproduction compared to their native range (such as the evolution of increased competitive ability hypothesis), in an effort to understand the causal drivers of invasion. Using diffuse knapweed (Centaurea diffusa) I assessed evolution in its invaded range in multiple ways. Chapter 2 describes two greenhouse common garden experiments that evaluated phenotypic and life history trait variation between the two ranges under benign and stressful conditions (drought, flooding, nutrient deficiency, and herbivory). Invasive individuals grew larger and flowered later in benign conditions, and performed as well or better under most of the tested stress conditions than native individuals. The strongest evidence for a trade-off in tolerance was exhibited under drought conditions, but only among native populations. Chapter 3 employs a field common garden to compare phenotypes, drought response, and adaptation to environmental conditions in a more natural setting. This study incorporates a large dataset of occurrence locations to look at the different relationships that populations in the two ranges have to their bioclimatic environments. I found that invasive C. diffusa individuals were larger, matured later, and have lost adaptation to environmental conditions apparent in native populations. More plastic invasive genotypes may have expanded the climatic niche inhabited in the invaded range. Chapter 4 attempts to identify a genetic mechanism underlying these phenotypic changes by comparing gene expression between the two ranges under benign and drought conditions. Genes were identified whose expression either varied constitutively or responded to drought stress differently between ranges. Based on these data, invasive populations may have constitutively higher levels of energy production, while native populations have a stronger cellular drought defense. This dissertation presents ample evidence of evolution in the invaded range and suggests that plasticity and rapid evolution had a significant impact on the successful invasion of North America by C. diffusa.

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Genomics of sunflower improvement from wild relatives to a global oil seed (2015)

Genetic diversity is a critical component of global food security. We depend on crop wild relatives as a genetic resource for the continued improvement and diversification of many crops. In this dissertation, I use population genomic approaches to investigate aspects of crop evolution in sunflower, which is a widely grown hybrid oilseed. In Chapter 1, the relevant aspects of crop improvement are reviewed, the sunflower system is introduced, and the research chapters are briefly described. In Chapter 2, I used transcriptome sequencing data to scan the genomes of a panel of cultivated and wild sunflowers and identified genes involved in domestication and improvement. Using data from additional wild sunflower species, I also identified widespread introgression of wild alleles into the modern crop gene pool. Chapter 3 describes a genomic survey of a diverse set of about 300 wild sunflower samples using genotyping by sequencing (GBS). The GBS data allowed me to determine evolutionary relationships and detect gene flow among taxa in the sunflower genus. I selected a subset of these wild samples to develop pre-bred lines, which I describe in Chapter 4. Pre-bred lines act as a bridge through which wild alleles may be introduced into breeding programs. Each of the circa 400 pre-bred lines I generated contain different components of their wild parent’s genome which were identified using GBS. Evaluation of these lines in Uganda revealed they could be excellent sources of alleles for disease resistance and drought tolerance. In Chapter 5, I examined relationships among cultivated lines, specifically the two heterotic groups that have been developed for hybrid crop production. Using whole genome sequencing data, I found many genomic regions were targets of selection during the development of these populations, and that patterns of diversity do not support an overdominance model of heterosis. Surprisingly, only two regions, which correspond to introduced wild alleles, are highly differentiated between these two populations. As I conclude in Chapter 6, the history of the use of wild relatives in sunflower breeding is found in the genomes of these plants, and permeates and defines modern lines.

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The Landscape of Divergence in Silverleaf Sunflowers (2015)

The Texas endemic silverleaf sunflower, Helianthus argophyllus, exhibits striking genetic variation in life history: some individuals flower in late summer and are relatively short, while other individuals delay flowering in favor of growth until fall. The central goal of this research is to identify and characterize the evolutionary drivers of this variation: either local adaptation under divergent natural selection, neutral phenotypic divergence resulting from reduced gene flow and subsequent genetic drift, or both. Helianthus argophyllus exhibits strong regional genetic structure. However, populations from the central area of the species range form a single genetic cluster but are split into two phenotypic clusters: mainland coast populations, which are primarily tall and late flowering, and barrier island populations, which contain short/early flowering and tall/later flowering individuals at roughly equal frequencies. Some traits, including floral size characters, are more differentiated across the species range than is expected based on neutral genetic divergence (QST > FST), a signal of local adaptation. In a reciprocal transplant experiment, barrier island plants had higher survival rates and overall fitness than non-local individuals at barrier island sites. Observations of selection in wild populations revealed directional selection for early flowering in barrier island populations that contrasts with selection for a later flowering optimum in mainland coast populations. Collectively, these analyses support a hypothesis of adaptive divergence in flowering time in H. argophyllus, although the ecological mechanism(s) and genetic basis of this divergence have yet to be explored.

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Patterns of domestication in the compositae and beyond (2012)

Domestication is the process of evolutionary change that results in the phenotypic and genetic differences between a crop species and its ‘wild’ progenitor. Domesticated species varywidely in their phylogenetic diversity, diversity of uses, and degree of domestication. Here, weattempt to better understand the traits and processes that govern this diversity of domesticatedspecies by taking a comparative view of domestication. First, we compare patterns ofdomestication in the Compositae family (chapter 2) and propose that the prevalence of secondarydefense compounds, the lack of carbohydrates that can be digested by the human gut, and thepredominantly mechanical or wind-dependent seed dispersal syndrome of the family are key reasons for the apparent paucity of crops in the Compositae family. We then report on the establishment of genomic tools and resources in the form of a library of expressed sequence tags, a set of microsatellite loci, and the full sequence of the chloroplast genome for one particular domesticated species in the Compositae, the oil-seed crop Noug (Guizotia abyssinica) (chapter 3). A combination of genotypic, phenotypic and eco-geographic analyses is then used to testwhether high levels of crop-wild gene flow and/or unfavorable phenotypic correlations are thereason why noug appears to be only semi-domesticated (chapter 4). Even though we did not findevidence for either of these hypotheses, our data revealed 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. We then suggest that domestication may also have been slowed by noug’s outcrossing mating system. The idea that transitions in mating systems and other reproductive barriers between crops and their wild progenitors play a role in domestication is then further explored in a systematic comparison of several crops of major economic importance within and beyond the Compositae family (chapter 5). The majority of such crops appear to indeed be isolated from their progenitors by one or more reproductive barriers, even in the absence of geographical isolation during domestication.

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Master's Student Supervision (2010 - 2020)
The First Reference Genome of Sunflower (Helianthus annuus L.) A Domesticated Compilospecies (2015)

I present the first reference genome for sunflower, Helianthus annuus. The reference is 3.6 billion base pairs long and is divided into seventeen lines of text representing the DNA of sunflower’s seventeen chromosomes. This reference was constructed via DNA sequencing and assembly of sunflower line HA412, physical mapping using a sequence-based barcoding approach, and genetic mapping based on low coverage DNA sequencing of a highly polymorphic mapping population. I also assembled and annotated a reference genome of sunflower’s mitochondrial genome. Sunflower and its wild relatives are a useful system for studying ecology and evolution. Helianthus annuus may be regarded as a natural compilospecies; adaptive introgressive hybridization with related species has facilitated the expansion of its range over a variety of soils and climates. In addition, the compatibility of sunflower with its extremophile wild relatives offers the opportunity to breed environmentally resilient sunflower cultivars that can cope with global climate change. The resource described in this thesis will be a useful tool for evolutionary biologists and crop breeders with interests pertaining to sunflower genetics.

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