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Rieseberg, L. H.

Publications and source records attributed to Rieseberg, L. H..

At least 37 records · Page 2Linked to original sources

Repeatability of adaptation in sunflowers: genomic regions harbouring inversions also drive adaptation in species lacking an inversion

Local adaptation commonly involves alleles of large effect, which experience fitness advantages when in positive linkage disequilibrium (LD). Because segregating inversions suppress recombination and facilitate the maintenance of LD between locally adapted loci, they are also commonly found to be associated with adaptive divergence. However, it is unclear what fraction of an adaptive response can be attributed to inversions and alleles of large effect, and whether the loci within an inversion could still drive adaptation in the absence of its recombination-suppressing effect. Here, we use genome-wide association studies to explore patterns of local adaptation in three species of sunflower: Helianthus annuus, H. argophyllus, and H. petiolaris, which each harbour a large number of species-specific inversions. We find evidence of significant genome-wide repeatability in signatures of association to phenotypes and environments, which are particularly enriched within regions of the genome harbouring an inversion in one species. This shows that while inversions may facilitate local adaptation, at least some of the loci can still harbour mutations that make substantial contributions without the benefit of recombination suppression in species lacking a segregating inversion. While a large number of genomic regions show evidence of repeated adaptation, most of the strongest signatures of association still tend to be species-specific, indicating substantial genotypic redundancy for local adaptation in these species.

evolutionary biology↗

Re-evaluating homoploid reticulate evolution in the annual sunflowers.

Sunflowers of the genus Helianthus are models for hybridization research and contain three of the best studied examples of homoploid hybrid speciation. To understand the broader picture of hybridization within the annual sunflowers, we used whole genome resequencing to conduct a phylogenomic analysis and test for gene flow between lineages. We find that all annual sunflower species tested have evidence of admixture, suggesting hybridization was common during the radiation of the genus. Support for the major species tree decreases with recombination rate, consistent with hybridization and introgression contributing to discordant topologies. Admixture graphs found hybridization to be associated with the origins of the three putative hybrid species (H. anomalus, H. deserticola, and H. paradoxus). However, the hybridization events are more ancient than suggested by previous work. Furthermore, H. anomalus and H. deserticola appear to have arisen from a single hybridization event involving an unexpected donor, rather than through multiple independent events as previously proposed. Using a broader data set that covers the whole Helianthus genus, including perennial species, we find that signals of introgression span the genus and beyond, suggesting highly divergent introgression and/or the sorting of ancient haplotypes. Thus, Helianthus can be viewed as a syngameon in which largely reproductively isolated species are linked together by occasional or frequent gene flow.

evolutionary biology↗

Chromosome-scale reference genome and RAD-based genetic map of yellow starthistle (Centaurea solstitialis) reveal putative structural variation and QTLs associated with invader traits

Invasive species offer outstanding opportunities to identify the genomic sources of variation that contribute to rapid adaptation, as well as the genetic mechanisms facilitating invasions. The Eurasian plant yellow starthistle (Centaurea solstitialis) is highly invasive in North and South American grasslands and known to have evolved increased growth and reproduction during invasion. Here we develop new genomic resources for C. solstitialis and map the genetic basis of invasiveness traits. We present a chromosome-scale (1N = 8) reference genome using PacBio CLR and Dovetail Omni-C technologies, and functional gene annotation using RNAseq. We find repeat structure typical of the family Asteraceae, with over 25% of gene content derived from ancestral whole genome duplications (paleologs). Using an F2 mapping population derived from a cross between native and invading parents, with a restriction site-associated DNA (RAD)-based genetic map, we validate the assembly and identify 13 QTL underpinning size traits that have evolved during invasion. We find evidence that large effect QTL may be associated with structural variants between native and invading genotypes, including a variant with an overdominant and pleiotropic effect on key invader traits. We also find evidence of significant paleolog enrichment under two QTL. Our results add to growing evidence of the importance of structural variants in evolution, and to understanding of the rapid evolution of invaders. Significance StatementInvasive species often evolve rapidly in new environments, potentially informing our understanding of the genomic basis of adaptation, but genomic studies of these non-model systems are limited. We provide a chromosome-scale reference genome, annotation, and genetic map for the invasive plant yellow starthistle, and we investigate the genetic basis of invader trait evolution in this system. We find regions of the genome with large effects on traits that differ between native and invading genotypes, and evidence suggesting genome structural variants and past genome duplications could play a role in rapid adaptation of invading populations. These genomic resources and evolutionary insights aid in our understanding of the sources of genomic variation for adaptation, and how their evolution facilitates invasion.

genomics↗

The western redcedar genome reveals low genetic diversity in a self-compatible conifer

We assembled the 9.8 Gbp genome of western redcedar (WRC, Thuja plicata), an ecologically and economically important conifer species of the Cupressaceae. The genome assembly, derived from a uniquely inbred tree produced through five generations of self-fertilization (selfing), was determined to be 86% complete by BUSCO analysis - one of the most complete genome assemblies for a conifer. Population genomic analysis revealed WRC to be one of the most genetically depauperate wild plant species, with an effective population size of approximately 300 and no significant genetic differentiation across its geographic range. Nucleotide diversity, {pi}, is low for a continuous tree species, with many loci exhibiting zero diversity, and the ratio of {pi} at zero-to four-fold degenerate sites is relatively high ([~] 0.33), suggestive of weak purifying selection. Using an array of genetic lines derived from up to five generations of selfing, we explored the relationship between genetic diversity and mating system. While overall heterozygosity was found to decline faster than expected during selfing, heterozygosity persisted at many loci, and nearly 100 loci were found to deviate from expectations of genetic drift, suggestive of associative overdominance. Non-reference alleles at such loci often harbor deleterious mutations and are rare in natural populations, implying that balanced polymorphisms are maintained by linkage to dominant beneficial alleles. This may account for how WRC remains responsive to natural and artificial selection, despite low genetic diversity.

plant biology↗

The genomics of linkage drag in sunflower

Crop wild relatives represent valuable sources of alleles for crop improvement, including adaptation to climate change and emerging diseases. However, introgressions from wild relatives might have deleterious effects on desirable traits, including yield, due to linkage drag. Here we comprehensively analyzed the genomic and phenotypic impacts of wild introgressions into cultivated sunflower to estimate the impacts of linkage drag. First, we generated new reference sequences for seven cultivated and one wild sunflower genotype, as well as improved assemblies for two additional cultivars. Next, relying on previously generated sequences from wild donor species, we identified introgressions in the cultivated reference sequences, as well as the sequence and structural variants they contain. We then used a ridge regression model to test the effects of the introgressions on phenotypic traits in the cultivated sunflower association mapping population. We found that introgression has introduced substantial sequence and structural variation into the cultivated sunflower gene pool, including > 3,000 new genes. While introgressions reduced genetic load at protein-coding sequences and positively affected traits associated with abiotic stress resistance, they mostly had negative impacts on yield and quality traits. Introgressions found at high frequency in the cultivated gene pool had larger effects than low frequency introgressions, suggesting that the former likely were targeted by artificial selection. Also, introgressions from more distantly related species were more likely to be maladaptive than those from the wild progenitor of cultivated sunflower. Thus, pre-breeding efforts should focus, as far as possible, on closely related and fully compatible wild relatives.

genomics↗

Large haploblocks underlie rapid adaptation in an invasive weed

Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. We leverage extensive contemporary and historical collections of Ambrosia artemisiifolia--an aggressively invasive weed and primary cause of pollen-induced hayfever--to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks-- indicative of chromosomal inversions--contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolias global spread across vast climatic gradients.

evolutionary biology↗

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

Biological invasions offer a unique opportunity to investigate evolution over contemporary time-scales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high-density linkage map (4,493 SNPs) and paired this with phenotypic data from an F2 mapping population (n=336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger and more tightly-linked alleles should underlie rapid local adaptation during invasion, particularly when divergently-adapting populations experience high-levels of gene flow.

evolutionary biology↗

Uncovering the hologenomic basis of an extraordinary plant invasion

While invasive species are a key driver of the global biodiversity crisis, the drivers of invasiveness remain debated. To investigate the genomic basis of invasiveness in plants, we use the invasive weed Ambrosia artemisiifolia, introduced to Europe in the late 19th century, resequencing 655 ragweed genomes, including 308 herbarium specimens collected up to 190 years ago. In introduced European populations, we report selection signatures in defense genes and lower prevalence of particular plant pathogens in the invasive range. Together with temporal changes in population structure associated with introgression from closely related Ambrosia species, escape from microbial enemies likely favoured the plants remarkable success as an invasive species. One-Sentence SummaryThe invasive success of European ragweed was facilitated by release from enemy microbes and inter-species hybridization.

genomics↗

High homozygosity of inversions in sunflower species largely averts accumulation of deleterious mutations

Recombination is critical both for accelerating adaptation and for the purging of deleterious mutations. Chromosomal inversions can act as recombination modifiers that suppress local recombination and, thus, are predicted to accumulate such mutations. In this study, we investigated patterns of recombination, transposable element abundance and coding sequence evolution across the genomes of 1,445 individuals from three sunflower species, as well as within nine inversions segregating within species. We also analyzed the effects of inversion genotypes on 87 phenotypic traits to test for overdominance. We found significant negative correlations of long terminal repeat retrotransposon abundance and deleterious mutations with recombination rates across the genome in all three species. However, we failed to detect an increase in these features in the inversions, except for a modest increase in the proportion of stop codon mutations in several very large or rare inversions. Moreover, there was little evidence of phenotypic overdominance in inversion heterozygotes, consistent with observations of minimal deleterious load. On the other hand, significantly greater load was observed for inversions in populations polymorphic for a given inversion compared to populations monomorphic for one of the arrangements, suggesting that the local state of inversion polymorphism affects deleterious load. These seemingly contradictory results can be explained by the geographic structuring and consequent excess homozygosity of inversions in wild sunflowers. Inversions contributing to local adaptation often exhibit geographic structure; such inversions represent ideal recombination modifiers, acting to facilitate adaptive divergence with gene flow, while largely averting the accumulation of deleterious mutations due to recombination suppression.

evolutionary biology↗

Genetic basis and dual adaptive role of floral pigmentation in sunflowers

Variation in floral displays, both between and within species, has been long known to be shaped by the mutualistic interactions that plants establish with their pollinators. However, increasing evidence suggests that abiotic selection pressures influence floral diversity as well. Here we analyze the genetic and environmental factors that underlie patterns of floral pigmentation in wild sunflowers. While sunflower inflorescences appear invariably yellow to the human eye, they display extreme diversity for patterns of ultraviolet pigmentation, which are visible to most pollinators. We show that this diversity is largely controlled by cis-regulatory variation at a single MYB transcription factor, HaMYB111, through accumulation of UV-absorbing flavonol glycosides. As expected, different patterns of ultraviolet pigments in flowers have a strong effect on pollinator preferences. However, variation for floral ultraviolet patterns is also associated with environmental variables, especially relative humidity, across populations of wild sunflowers. Larger ultraviolet patterns, which are found in drier environments, limit transpiration, therefore reducing water loss. The dual role of floral UV patterns in pollination attraction and abiotic responses reveals the complex adaptive balance underlying the evolution of floral traits.

evolutionary biology↗

Global mismatches between crop distributions and climate suitability

The selection of new crops and the migration of crop areas are two key strategies for agriculture to cope with climate change and ensure food security in the coming years. However, both rely on the assumption that climate is a major factor determining crop distributions worldwide. Here, we show that the current global distributions of nine of twelve major crops strongly diverge from their modelled climatic suitability for yields, after controlling for technology, agricultural management and soil conditions. Comparing the climatic niches of crops and their wild progenitors reveals that climate suitability is higher outside the native climatic range for six of these nine crops while all of them are farmed predominantly in their native ranges. These results show that agricultural strategies coping with climate change will be unsuccessful unless they fully consider the social, cultural, and ecological factors underpinning crop distributions.

ecology↗

A draft genome of Alliaria petiolata (garlic mustard) as a model system for invasion genetics

The emerging field of invasion genetics examines the genetic causes and consequences of biological invasions, but few study systems are available that integrate deep ecological knowledge with genomic tools. Here we report on the de novo assembly and annotation of a genome for the biennial herb Alliaria petiolata (M. Bieb.) Cavara & Grande (Brassicaceae), which is widespread in Eurasia and invasive across much of temperate North America. Our goal was to sequence and annotate a genome to complement resources available from hundreds of published ecological studies, a global field survey, and hundreds of genetic lines maintained in Germany and Canada. We sequenced a genotype (EFCC-3-20) collected from the native range near Venice, Italy and sequenced paired-end and mate pair libraries at ~70 x coverage. A de novo assembly resulted in a highly continuous draft genome (N50 = 121 Mb; L50 = 2) with 99.7 % of the 1.1 Gb genome mapping to scaffolds of at least 50 Kb in length. A total of 64,770 predicted genes in the annotated genome include 99 % of plant BUSCO genes and 98 % of transcriptome reads. Consistent with previous reports of (auto)hexaploidy in western Europe, we found that almost one third of BUSCO genes (390/1440) mapped to two or more scaffolds despite < 2 % genome-wide average heterozygosity. The continuity and gene space quality of our draft assembly will enable molecular and functional genomic studies of A. petiolata to address questions relevant to invasion genetics and conservation strategies.

genomics↗

An unexpected donor in the adaptive introgression candidate Helianthus annuus subsp. texanus.

Hybridization is widely acknowledged as an important mechanism of acquiring adaptive variation. In Texas, the sunflower Helianthus annuus subsp. texanus is thought to have acquired herbivore resistance and morphological traits via introgression from a local congener, H. debilis. Here we test this hypothesis using whole genome sequencing data from across the entire range of H. annuus and possible donor species, as well as phenotypic data from a common garden study. We find that although it is morphologically convergent with H. debilis, H. a. texanus has conflicting signals of introgression. Genome wide tests (Pattersons D and TreeMix) only find evidence of introgression from H. argophyllus (sister species to H. annuus and also sympatric), but not H. debilis, with the exception of one individual of 109 analysed. We further scanned the genome for localized signals of introgression using PCAdmix and found minimal but non-zero introgression from H. debilis and significant introgression from H. argophyllus. Putative introgressions mainly occur in high recombination regions as predicted by theory if introgressed ancestry contains maladaptive alleles. To reconcile the disparate findings of our analyses, we discuss potential test-specific confounding features, including introgression from other taxa. Given the paucity of introgression from H. debilis, we argue that the morphological convergence observed in Texas is likely independent of introgression.

evolutionary biology↗

Aberrant regulation of RNA splicing in sunflower hybrids may underlie intrinsic incompatibilities

Alternative spicing is an integral part of gene expression in multicellular organisms that allows for diverse mRNA transcripts and proteins to be produced from a single gene. However, most existing analyses have focused on macro-evolution, with only limited research on splice site evolution over shorter term, micro-evolutionary time scales. Here we examine splicing evolution that has occurred during domestication and observe 45 novel splice forms with strongly transgressive isoform compositions, representing 0.24% of analyzed transcripts. We identify loci associated with variation in the levels of these splice forms, finding that many novel transcripts were regulated by multiple alleles with non-additive interactions. A subset of these interactions involved the expression of individual spliceosome components. These overdominant and epistatic interactions often resulted in alteration in the protein-coding regions of the transcripts, resulting in frameshifts and truncations. By associating the splice variation in these genes with size and growth rate measurements, we found that none of the individual splice variants affected these plant traits significantly, but the cumulative expression of all aberrant transcripts did show a significant reduction in growth rate associated with higher proportions of disrupted transcripts. This demonstrates the importance of co-evolution of the different spliceosomal components and their regulators and suggests that these genes may contribute to evolution of reproductive isolation as Bateson-Dobzhansky-Muller incompatibility loci. Author summaryIn multicellular organisms, it is common that segments of pre-mRNA molecules are physically removed, and the remaining segments are spliced back together. Through splicing alternative combinations of segments together, organisms produce various mRNA molecules, and thus multiple proteins, using the information encoded in a single gene. Here, we investigated the RNA of two sunflower genotypes, one wild and one domesticated, as well as the hybrid offspring resulting from a cross between the two genotypes. We found certain mRNA molecules that were spliced exclusively in the hybrids and were absent in the examined parental lines. These unique hybrid mRNAs were predicted to be consequential for the hybrids health, and thus represented a malfunction in the mechanisms that regulate splicing. These results improve our understanding of the genetic regulation of alternative splicing and how alternative splice forms evolve. Our findings may lead to further inquiries about how aberrant splicing promotes the formation of new species in nature.

evolutionary biology↗

Contrasting selection at multiple life stages maintains divergent adaptation between sunflower ecotypes

Conspecific populations living in adjacent, but contrasting, microenvironments represent excellent systems for studying natural selection. These systems are valuable because gene flow maintains genetic homogeneity except at loci experiencing strong, divergent selection. A history of reciprocal transplant and common garden studies in such systems, and a growing number of genomic studies, have contributed to understanding how selection operates in natural populations. While selection can vary across different fitness components and life stages, few studies have investigated how this ultimately affects allele frequencies and persistence of divergent populations. Here, we study two sunflower ecotypes in distinct, adjacent habitats by combining demographic models with genome-wide sequence data to estimate fitness components, absolute fitness, and allele frequency change at multiple life stages. This framework allows us to demonstrate that only local ecotypes experience positive population growth (lambda>1) and that the maintenance of divergent adaptation is mediated via habitat- and life stage-specific selection. We identify genetic variation, significantly driven by loci in chromosomal inversions, associated with different life history strategies in neighbouring ecotypes that optimize different fitness components and contribute to the persistence of each ecotype in its respective habitat.

evolutionary biology↗

Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype

Both models and case studies suggest that chromosomal inversions can facilitate adaptation and speciation in the presence of gene flow by suppressing recombination between locally adapted alleles. Until recently, however, it has been laborious and time-consuming to identify and genotype inversions in natural populations. Here we apply RAD sequencing data and newly developed population genomic approaches to identify putative inversions that differentiate a sand dune ecotype of the prairie sunflower (Helianthus petiolaris) from populations found on the adjacent sand sheet. We detected seven large genomic regions that exhibit a different population structure than the rest of the genome and that vary in frequency between dune and non-dune populations. These regions also show high linkage disequilibrium and high heterozygosity between, but not within haplotypes, consistent with the behavior of large inversions, an inference subsequently validated in part by comparative genetic mapping. Genome-environment association analyses show that key environmental variables, including vegetation cover and soil nitrogen, are significantly associated with inversions. The inversions co-locate with previously described \"islands of differentiation,\" and appear to play an important role in adaptive divergence and incipient speciation within H. petiolaris.

evolutionary biology↗

Patterns, predictors, and consequences of dominance in hybrids

Are first-generation (F1) hybrids typically intermediate for all traits that differentiate their parents? Or are they similar to one parent for most traits, or even mismatched for divergent traits? Although the phenotype of otherwise viable and fertile hybrids determines their fate, little is known about the general patterns, predictors, and consequences of phenotype expression in hybrids. To address this empirical gap, we compiled data from nearly 200 studies where traits were measured in a common environment for two parent populations and F1 hybrids. We find that individual traits are typically halfway between the parental midpoint and one parental value (i.e., hybrid trait values are typically 0.25 or 0.75 if parents values are 0 & 1). When considering pairs of traits together, a hybrids multivariate phenotype tends to resemble one parent (pairwise parent-bias) about 50 % more than the other while also exhibiting a similar magnitude of trait 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--where there is among-individual variation in dominance and mismatch due to segregation of divergent alleles--we illustrate that pairwise parent-bias improves fitness while mismatch reduces fitness. Importantly, the effect of mismatch on fitness was stronger than that of pairwise parent-bias. In sum, our study has three major conclusions. First, hybrids between ecologically divergent natural populations are typically not phenotypically intermediate but rather exhibit substantial mismatch while also resembling one parent more than the other. Second, dominance and mismatch are likely determined by population-specific processes rather than general rules. Finally, selection against hybrids likely results from both selection against somewhat intermediate phenotypes and against mismatched trait combinations.

evolutionary biology↗

Massive haplotypes underlie ecotypic differentiation in sunflowers

Species often include multiple ecotypes that are adapted to different environments. But how do ecotypes arise, and how are their distinctive combinations of adaptive alleles maintained despite hybridization with non-adapted populations? Re-sequencing of 1506 wild sunflowers from three species identified 37 large (1-100 Mbp), non-recombining haplotype blocks associated with numerous ecologically relevant traits, and soil and climate characteristics. Limited recombination in these regions keeps adaptive alleles together, and we find that they differentiate several sunflower ecotypes; for example, they control a 77 day difference in flowering between ecotypes of silverleaf sunflower (likely through deletion of a FLOWERING LOCUS T homolog), and are associated with seed size, flowering time and soil fertility in dune-adapted sunflowers. These haplotypes are highly divergent, associated with polymorphic structural variants, and often appear to represent introgressions from other, possibly extinct, congeners. This work highlights a pervasive role of structural variation in maintaining complex ecotypic adaptation.

evolutionary biology↗