DarwinPlants: Probing the genomic basis of rapid evolutionary diversification in the Galápagos daisy trees (genus Scalesia)

This project sought to understand the genetic basis of the rapid evolution of diversity in a unique and threatened group of plants from the Galápagos Islands. Studies of the forms and distribution patterns of species on the world's oceanic island chains have provided scientists with major insights into the process of evolution. Among these chains is the Galápagos archipelago, where Charles Darwin collected the specimens and observations that would eventually lead to the formation of his theory of evolutionary change through natural selection. Daisy trees (genus Scalesia) are one special group of plants found only on the Galápagos islands. Within a relatively small time period (four million years), the plants evolved from a single ancestor into 15 different species with drastic variation in size and shape, as well as diversity of life habits and strategies. For this reason, these plants have been called 'the Darwin's finches of the plant world'. The main objective of our project was to determine the genetic mechanisms that have allowed such a rapid and dramatic diversification in this group. Our team used several advanced approaches to determine these mechanisms, including next-generation sequencing of entire genomes (DNA) and transcriptomes (RNA) contained in hundreds of individual plants. We used this data to apply phylogenetic, population genetic, and evolutionary genomic methods to achieve our secondary objective, to reconstruct the evolutionary history of all of the Scalesia species. The project generated a large amount of data that will continue to be analyzed for years to come. These data include a chromosome-scale de-novo reference genome for Scalesia atractyloides, a detailed understanding of the timing/nature of the hybridization event that led to the genus, as well as ~400 resequenced Scalesia genomes, 5 PacBio-based transcriptome assemblies from various Scalesia species, and ~200 resequenced transcriptomes from 6 Scalesia species. Three postdoctoral researchers worked on the project. Project members have given at least ten academic lectures/seminars describing the project and disseminating its main results. Several publications have resulted from the project so far, including: (1) an article describing a high-quality reference genome assembly for Scalesia atractyloides, as well as the genomic basis of the Scalesia plants' adaptation to the island environment, published in Nature Communications (https://doi.org/10.1038/s41467-022-31280-w), and (2) an article describing how genomics can inform open questions in adaptive radiations, published in Trends in Ecology and Evolution (https://doi.org/10.1016/j.tree.2023.02.003). More publications are on the way.

The significance of the DarwinPlants project will be felt most keenly in the fields of genome evolutionary biology, and biodiversity conservation. In the field of genome evolutionary biology, this project produced the highest-quality non-model, non-crop plant genome assembly to-date, and thus our publications will serve as a guidepost for future efforts to assemble and analyze larger and more complicated plant genomes. The project also characterized, for the first time and in an unbiased way, the genetic basis for the ‘island syndrome’ in a plant lineage. The project also analyzed the evolutionary genomics of the adaptive trait (leaf morphology) at the root of a textbook adaptive radiation. It is thus expected that this work, via its publications in highly regarded international journals, will be highly cited by the scientific community. The project also trained three post-graduate researchers to develop and use cutting-edge methods in evolutionary genomics, and increased their scientific networks considerably, thus establishing an upward trajectory for their research careers in Norway or abroad. Toward the conservation of the Galapagos-endemic Scalesia plants, some of which are highly threatened and critically endangered, our work provides results that can be used by wildlife/biodiversity managers. Our genomic analyses have clearly shown that in extant Scalesia species, as well as several populations within species that occur on multiple islands, in almost every case inter-population gene flow ceased long ago. This tendency toward long-term isolation implies that almost every discrete population is already on its own evolutionary trajectory, and that there are more Scalesia species than were previously described. Thus our conservation recommendation is that each physically isolated Scalesia population should be protected, as each will likely become a new species given enough time. The project work also clearly shows that particular populations/species have very low genetic diversity and are thus more vulnerable to future threats.

Within the last 4M years, the endemic Galápagos daisy trees rapidly diversified from a weedy ancestor into genus Scalesia, which contains at least 15 species with spectacularly divergent life history traits and variation in the size and shape of their leaves. While Darwin’s finches of Galápagos have become a model of adaptive radiation, these plants have received remarkably little attention despite their even more dramatic radiation into diverse ecological niches. More curious is that this rapid diversification seems to have generated little genetic diversity on which evolution might act. Considering its importance in plant evolution, polyploidy may have played have a role. Novel next-generation sequencing technologies are revolutionizing evolutionary genetic studies of non-model organisms. We propose to generate an annotated reference genome assembly for Scalesia as well as whole-genome sequencing data from population samples representing all species, subspecies, and hybrid populations of these threatened plants. We will apply novel transcriptomic, phylogenomic, and population genomic analysis approaches to this data in order to determine how minimal genetic variation could generate enormous morphological diversity, and which regions of genome underlie this diversity. Specifically, DarwinPlants will test hypotheses that despite overall low genomic diversity in Scalesia, rapid diversification of these plants was enabled by both multiple bouts of inter-specific introgression and subtle changes in gene expression networks related to leaf development, light, and stress. DarwinPlants will generate fundamental insights into the genetic processes underlying rapid diversification and ecological speciation of plants, as well as new population genetic approaches for characterizing inter-population differentiation in genomic data from polyploid organisms.