Documenting homoploid hybrid speciation.

Homoploid hybrid speciation is challenging to document because hybridization can lead to outcomes other than speciation. Thus, some authors have argued that establishment of homoploid hybrid speciation should include evidence that reproductive barriers isolating the hybrid neo-species from its parental species were derived from hybridization. While this criterion is difficult to satisfy, several recent papers have successfully employed a common pipeline to identify candidate genes underlying such barriers and (in one case) to validate their function. We describe this pipeline, its application to several plant and animal species and what we have learned about homoploid hybrid speciation as a consequence. We argue that - given the ubiquity of admixture and the polygenic basis of reproductive isolation - homoploid hybrid speciation could be much more common and more protracted than suggested by earlier conceptual arguments and theoretical studies.

How Does Selfing Affect the Pace and Process of Speciation?

Surprisingly little attention has been given to the impact of selfing on speciation, even though selfing reduces gene flow between populations and affects other key population genetics parameters. Here we review recent theoretical work and compile empirical data from crossing experiments and genomic and phylogenetic studies to assess the effect of mating systems on the speciation process. In accordance with theoretical predictions, we find that accumulation of hybrid incompatibilities seems to be accelerated in selfers, but there is so far limited empirical support for a predicted bias toward underdominant loci. Phylogenetic evidence is scarce and contradictory, including studies suggesting that selfing either promotes or hampers speciation rate. Further studies are therefore required, which in addition to measures of reproductive barrier strength and selfing rate should routinely include estimates of demographic history and genetic divergence as a proxy for divergence time.

Development and characterization of a new sunflower source of resistance to race G of Orobanche cumana Wallr. derived from Helianthus anomalus.

KEY MESSAGE: A new OrAnom1 gene introgressed in cultivated sunflower from wild Helianthus anomalus confers late post-attachment resistance to Orobanche cumana race G and maps to a target interval in Chromosome 4 where two receptor-like kinases (RLKs) have been identified in the H. anomalus genome as putative candidates. Sunflower broomrape is a parasitic weed that infects sunflower (Helianthus annuus L.) roots causing severe yield losses. Breeding for resistance is the most effective and sustainable control method. In this study, we report the identification, introgression, and genetic and physiological characterization of a new sunflower source of resistance to race G of broomrape developed from the wild annual sunflower H. anomalus (accession PI 468642). Crosses between PI 468642 and the susceptible line P21 were carried out, and the genetic study was conducted in BC1F1, BC1F2, and its derived BC1F3 populations. A BC1F5 germplasm named ANOM1 was developed through selection for race G resistance and resemblance to cultivated sunflower. The resistant trait showed monogenic and dominant inheritance. The gene, named OrAnom1, was mapped to Chromosome 4 within a 1.2 cM interval and co-segregated with 7 SNP markers. This interval corresponds to a 1.32 Mb region in the sunflower reference genome, housing a cluster of receptor-like kinase and receptor-like protein (RLK-RLP) genes. Notably, the analysis of the H. anomalus genome revealed the absence of RLPs in the OrAnom1 target region but featured two RLKs as possible OrAnom1 candidates. Rhizotron and histological studies showed that OrAnom1 determines a late post-attachment resistance mechanism. Broomrape can establish a vascular connection with the host, but parasite growth is stopped before tubercle development, showing phenolic compounds accumulation and tubercle necrosis. ANOM1 will contribute to broadening the genetic basis of broomrape resistance in the cultivated sunflower pool and to a better understanding of the molecular basis of the sunflower-broomrape interaction.

Repeatability of adaptation in sunflowers reveals that 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, Helianthus argophyllus, and Helianthus 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.

In plants, like in humans, DNA is arranged into sections known as genes that are in turn organised into structures called chromosomes. Mutations that modify the activity of these genes can help plant species to adapt to a new environment or to extreme conditions such as drought. However, successful adaptation often requires changes in many different genes. If these sets of genes are located close to each other on the same chromosome, any mutations will likely be passed onto the next generation together. If the genes are located further away, or even on different chromosomes, they may instead be inherited separately so that the next generation does not benefit as much from the adaptation. A chromosome inversion ­ when a segment of chromosome breaks off and reattaches the other way around ­ can increase the likelihood that sets of mutations on the same chromosome will be inherited together. Many previous studies have found that chromosome inversions tend to drive the ability of species to adapt to different environments by keeping together mutations that affect the same characteristics. However, it is not clear how inversions affect the repeatability of the adaptation, that is, if another group of closely related plants faced the same challenge in their environment would they evolve in the same way, or would they evolve a new response? To address this question, Soudi, Jahani et al. used a genetics approach known as a genome wide association study to explore how three closely related species of sunflower have adapted to their respective environments. Two of the species grow in various environments across the centre and west of the USA that are often hot and dry, whereas the third species is restricted to the more humid coastal plain of Texas, USA. The experiments found that a few key genes had changed in all three sunflower species. However, each species also had mutations in a larger set of unique genes that were not changed in the other species. Regions of chromosomes harbouring inversions in one of the species tended to have more of the key genes within them, compared to other genomic regions. This was also true for species that did not have inversions in those regions. This demonstrates that genes in regions affected by chromosome inversions can still help plants adapt to changes in the environment even in the absence of inversions. Sunflowers are widely grown for their edible oily seeds. In the future, some of the key genes identified in this work may be useful candidates for plant breeding to improve the resilience of sunflowers to drought, high temperatures and other environmental challenges.

Temporal collections to study invasion biology.

Biological invasions represent an extraordinary opportunity to study evolution. This is because accidental or deliberate species introductions have taken place for centuries across large geographical scales, frequently prompting rapid evolutionary transitions in invasive populations. Until recently, however, the utility of invasions as evolutionary experiments has been hampered by limited information on the makeup of populations that were part of earlier invasion stages. Now, developments in ancient and historical DNA technologies, as well as the quickening pace of digitization for millions of specimens that are housed in herbaria and museums globally, promise to help overcome this obstacle. In this review, we first introduce the types of temporal data that can be used to study invasions, highlighting the timescale captured by each approach and their respective limitations. We then discuss how ancient and historical specimens as well as data available from prior invasion studies can be used to answer questions on mechanisms of (mal)adaptation, rates of evolution, or community-level changes during invasions. By bridging the gap between contemporary and historical invasive populations, temporal data can help us connect pattern to process in invasion science. These data will become increasingly important if invasions are to achieve their full potential as experiments of evolution in nature.

Crop adaptation to climate change: An evolutionary perspective.

The disciplines of evolutionary biology and plant and animal breeding have been intertwined throughout their development, with responses to artificial selection yielding insights into the action of natural selection and evolutionary biology providing statistical and conceptual guidance for modern breeding. Here we offer an evolutionary perspective on a grand challenge of the 21st century: feeding humanity in the face of climate change. We first highlight promising strategies currently under way to adapt crops to current and future climate change. These include methods to match crop varieties with current and predicted environments and to optimize breeding goals, management practices, and crop microbiomes to enhance yield and sustainable production. We also describe the promise of crop wild relatives and recent technological innovations such as speed breeding, genomic selection, and genome editing for improving environmental resilience of existing crop varieties or for developing new crops. Next, we discuss how methods and theory from evolutionary biology can enhance these existing strategies and suggest novel approaches. We focus initially on methods for reconstructing the evolutionary history of crops and their pests and symbionts, because such historical information provides an overall framework for crop-improvement efforts. We then describe how evolutionary approaches can be used to detect and mitigate the accumulation of deleterious mutations in crop genomes, identify alleles and mutations that underlie adaptation (and maladaptation) to agricultural environments, mitigate evolutionary trade-offs, and improve critical proteins. Continuing feedback between the evolution and crop biology communities will ensure optimal design of strategies for adapting crops to climate change.

Genomics of plant speciation.

Studies of plants have been instrumental for revealing how new species originate. For several decades, botanical research has complemented and, in some cases, challenged concepts on speciation developed via the study of other organisms while also revealing additional ways in which species can form. Now, the ability to sequence genomes at an unprecedented pace and scale has allowed biologists to settle decades-long debates and tackle other emerging challenges in speciation research. Here, we review these recent genome-enabled developments in plant speciation. We discuss complications related to identification of reproductive isolation (RI) loci using analyses of the landscape of genomic divergence and highlight the important role that structural variants have in speciation, as increasingly revealed by new sequencing technologies. Further, we review how genomics has advanced what we know of some routes to new species formation, like hybridization or whole-genome duplication, while casting doubt on others, like population bottlenecks and genetic drift. While genomics can fast-track identification of genes and mutations that confer RI, we emphasize that follow-up molecular and field experiments remain critical. Nonetheless, genomics has clarified the outsized role of ancient variants rather than new mutations, particularly early during speciation. We conclude by highlighting promising avenues of future study. These include expanding what we know so far about the role of epigenetic and structural changes during speciation, broadening the scope and taxonomic breadth of plant speciation genomics studies, and synthesizing information from extensive genomic data that have already been generated by the plant speciation community.

Evolutionary genomics of oceanic island radiations.

A recurring feature of oceanic archipelagos is the presence of adaptive radiations that generate endemic, species-rich clades that can offer outstanding insight into the links between ecology and evolution. Recent developments in evolutionary genomics have contributed towards solving long-standing questions at this interface. Using a comprehensive literature search, we identify studies spanning 19 oceanic archipelagos and 110 putative adaptive radiations, but find that most of these radiations have not yet been investigated from an evolutionary genomics perspective. Our review reveals different gaps in knowledge related to the lack of implementation of genomic approaches, as well as undersampled taxonomic and geographic areas. Filling those gaps with the required data will help to deepen our understanding of adaptation, speciation, and other evolutionary processes.

The genomics of linkage drag in inbred lines of 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 analyzed the genomic and phenotypic impacts of wild introgressions in inbred lines of cultivated sunflower to estimate the impacts of linkage drag. First, we generated 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 best linear unbiased prediction (BLUP) 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, 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, breeding efforts should focus, as far as possible, on closely related and fully compatible wild relatives.

Large haploblocks underlie rapid adaptation in the invasive weed Ambrosia artemisiifolia.

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. Here, 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. artemisiifolia's global spread across vast climatic gradients.

Re-evaluating Homoploid Reticulate Evolution in Helianthus 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 a 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 increasing 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 (Helianthus anomalus, Helianthus deserticola, and Helianthus 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. This means our results are consistent with, but not definitive proof of, two ancient independent homoploid hybrid speciation events in the genus. 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.

Replicated Evolution in Plants.

Similar traits and functions commonly evolve in nature. Here, we explore patterns of replicated evolution across the plant kingdom and discuss the processes responsible for such patterns. We begin this review by defining replicated evolution and the theoretical, genetic, and ecological concepts that help explain it. We then focus our attention on empirical cases of replicated evolution at the phenotypic and genotypic levels. We find that replication at the ecotype level is common, but evidence for repeated ecological speciation is surprisingly sparse. On the other hand, the replicated evolution of ecological strategies and physiological mechanisms across similar biomes appears to be pervasive. We conclude by highlighting where future efforts can help us bridge the understanding of replicated evolution across different levels of biological organization. Earth's landscape is diverse but also repeats itself. Organisms seem to have followed suit.

Expression complementation of gene presence/absence polymorphisms in hybrids contributes importantly to heterosis in sunflower.

INTRODUCTION: Numerous crops have transitioned to hybrid seed production to increase yields and yield stability through heterosis. However, the molecular mechanisms underlying heterosis and its stability across environments are not yet fully understood. OBJECTIVES: This study aimed to (1) elucidate the genetic and molecular mechanisms underlying heterosis in sunflower, and (2) determine how heterosis is maintained under different environments. METHODS: Genome-wide association (GWA) analyses were employed to assess the effects of presence/absence variants (PAVs) and stop codons on 16 traits phenotyped in the sunflower association mapping population at three locations. To link the GWA results to transcriptomic variation, we sequenced the transcriptomes of two sunflower cultivars and their F1 hybrid (INEDI) under both control and drought conditions and analyzed patterns of gene expression and alternative splicing. RESULTS: Thousands of PAVs were found to affect phenotypic variation using a relaxed significance threshold, and at most such loci the "absence" allele reduced values of heterotic traits, but not those of non-heterotic traits. This pattern was strengthened for PAVs that showed expression complementation in INEDI. Stop codons were much rarer than PAVs and less likely to reduce heterotic trait values. Hybrid expression patterns were enriched for the GO category, sensitivity to stimulus, but all genotypes responded to drought similarily - by up-regulating water stress response pathways and down-regulating metabolic pathways. Changes in alternative splicing were strongly negatively correlated with expression variation, implying that alternative splicing in this system largely acts to reinforce expression responses. CONCLUSION: Our results imply that complementation of expression of PAVs in hybrids is a major contributor to heterosis in sunflower, consistent with the dominance model of heterosis. This mechanism can account for yield stability across different environments. Moreover, given the much larger numbers of PAVs in plant vs. animal genomes, it also offers an explanation for the stronger heterotic responses seen in the former.

HeliantHOME, a public and centralized database of phenotypic sunflower data.

Genomic studies often attempt to link natural genetic variation with important phenotypic variation. To succeed, robust and reliable phenotypic data, as well as curated genomic assemblies, are required. Wild sunflowers, originally from North America, are adapted to diverse and often extreme environments and have historically been a widely used model plant system for the study of population genomics, adaptation, and speciation. Moreover, cultivated sunflower, domesticated from a wild relative (Helianthus annuus) is a global oil crop, ranking fourth in production of vegetable oils worldwide. Public availability of data resources both for the plant research community and for the associated agricultural sector, are extremely valuable. We have created HeliantHOME ( http://www.helianthome.org ), a curated, public, and interactive database of phenotypes including developmental, structural and environmental ones, obtained from a large collection of both wild and cultivated sunflower individuals. Additionally, the database is enriched with external genomic data and results of genome-wide association studies. Finally, being a community open-source platform, HeliantHOME is expected to expand as new knowledge and resources become available.

Adaptation to distinct habitats is maintained by contrasting selection at different life stages in sunflower ecotypes.

Conspecific populations living in adjacent but contrasting microenvironments represent excellent systems for studying natural selection. These systems are valuable because gene flow is expected to force genetic homogeneity except at loci experiencing 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 the maintenance of divergence between populations. Here, we study two sunflower ecotypes in distinct, adjacent habitats by combining demographic models with genome-wide sequence data to estimate fitness and allele frequency change at multiple life stages. This framework allows us to estimate that only local ecotypes are likely to experience positive population growth (λ > 1) and that the maintenance of divergent adaptation appears to be 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 may contribute to the maintenance of distinct ecotypes.

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, π, is low for a continuous tree species, with many loci showing zero diversity, and the ratio of π at zero- to fourfold degenerate sites is relatively high (approximately 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. Although 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. Nonreference 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.

Matches and mismatches between the global distribution of major food crops and climate suitability.

Over the course of history, humans have moved crops from their regions of origin to new locations across the world. The social, cultural and economic drivers of these movements have generated differences not only between current distributions of crops and their climatic origins, but also between crop distributions and climate suitability for their production. Although these mismatches are particularly important to inform agricultural strategies on climate change adaptation, they have, to date, not been quantified consistently at the global level. Here, we show that the relationships between the distributions of 12 major food crops and climate suitability for their yields display strong variation globally. After investigating the role of biophysical, socio-economic and historical factors, we report that high-income world regions display a better match between crop distribution and climate suitability. In addition, although crops are farmed predominantly in the same climatic range as their wild progenitors, climate suitability is not necessarily higher there, a pattern that reflects the legacy of domestication history on current crop distribution. Our results reveal how far the global distribution of major crops diverges from their climatic optima and call for greater consideration of the multiple dimensions of the crop socio-ecological niche in climate change adaptive strategies.