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Advancing beyond the adaptive radiation paradigm: uncovering the contributions of adaptive and non-adaptive processes to a rapid plant radiation

Periodic Reporting for period 1 - RadiPhyte (Advancing beyond the adaptive radiation paradigm: uncovering the contributions of adaptive and non-adaptive processes to a rapid plant radiation)

Reporting period: 2019-09-01 to 2021-08-31

RadiPhyte focuses on a key question in evolutionary biology and a key aspect for our understanding of biodiversity through a ground-breaking investigation of the main triggers of one of the most rapid plant radiations known to science, the diversification of the genus Dianthus in Eurasia. The current paradigm on species radiations is that adaptation to different ecological niches together with the rise of phenotypic diversity trigger such rapid radiations. However, existing studies fail to test the alternative hypothesis, which is that rapid radiations could be also driven by non-adaptive processes mediated, for example by the geographic isolation of lineages with similar ecological niches. Therefore, in order to address the importance of adaptive versus non-adaptive processes in plant radiations, an evolutionary study of ecological and phenotypic differentiation in such a rapid radiation is required. Advanced genomic and phenotyping approaches, together with an accurate analytical framework, can reveal the processes that drive evolutionary radiations, and thereby enhance our understanding of macroevolution.
We chose to work on the Dianthus of Eurasia because they are truly the “cichlids of the plant world”. The genus Dianthus comprises >330 species distributed throughout temperate Eurasia and Africa, with the bulk of its diversity (≥245 species) occurring in continental Eurasia. Dianthus displays a striking morphological diversity, indicating that ecological adaptation has probably contributed to its radiation. The rapid radiation of Dianthus further appears to coincide with increased aridity and seasonality in the Mediterranean and Irano-Turanian bioregions. The two bioregions where most Dianthus species occur, the Mediterranean and Irano-Turanian regions, are among the globe’s most topographically complex areas. They are home to >20% of the world’s plant species and represent hotspots of evolutionary and biological diversity of the Old World.
The main objective of RadiPhyte was therefore to investigate the radiation patterns of the genus Dianthus through two simultaneous cutting-edge approaches: (1) modern high-throughput capture sequencing to generate a robust, fully resolved phylogeny of the genus and (2) phenotyping methods to acquire a vast 3D quantitative shape dataset of the flowers of the genus.
RadiPhyte made use of a novel approach to quantify 3-dimentional (3D) floral phenotypes from herbarium collection, which was developed during the project. Thanks to this novel approach, RadiPhyte is the first large scale 3D geometric morphometric study on flowers, which together with expansive genomic data, allows the first macro-evolutionary test of how morphological innovations open new adaptive zones and promote radiation. Our extensive sampling of the diversity of the group under study, made it possible to test how the group evolved across geographic space and determine the relative amount of adaptive versus non-adaptive radiation. Despite numerous problems caused by the Covid-19 epidemic, we could sample ≥ 200 species of Dianthus instead of the 150 planned; the task was thus completed beyond expectations. The sampling covered the geographic, phenotypic, as well as the phylogenetic diversity of the genus. Our study was the first to include species from remote areas of the Middle East and Central Asia; this approach provided us with a complete picture of the spectacular radiation of Dianthus into the arid mountain habitats of the latter regions.
We employed customized Target Capture Sequencing (TCS), which allowed us to successfully sequence herbarium material of Dianthus. In total DNA for 285 taxa was successfully extracted, of which 277 Dianthus specimens. In order to gather 3D flower datasets from compressed herbarium specimens, we successfully developed a new protocol to restore their shape. Flowers of >120 species of Dianthus were imaged and digitized; this unique phenotypic dataset is ready to be integrated together with our phylogenomic tree to elucidate radiation patterns in Dianthus. Moreover, our novel flower phenotypic methods allowed us to address previously unanswered questions about the phenotypic variation and evolution of flowers. In addition to sampling at the genus level, we also sampled at the individual and population levels. Our sampling allowed us to elucidate patterns of shape variation (i.e. modularity) across levels and uncover new relationships between these levels. Thanks to our extensive sampling of the genomic and phenotypic diversity of Dianthus across Eurasia, the results of our analyses on the radiation patterns of the genus appear robust and promising.
The overall goal of the dissemination activities of RadiPhyte was and is a wide-reaching impact, uptake and use of the project deliverables among target audiences: scientists, institutions, and the general public. The dissemination activities focused and currently still focus on three channels: project publications, event attendance, and online activities. Most of our dissemination activities were interrupted by the Covid-19 pandemic and postponed to 2022. The outcomes of RadiPhyte will produce at least four scientific papers of interest to the scientific community; our results are currently under review in high-impact specialist evolutionary ecology journal, and further three papers are in preparation.
RadiPhyte not only allows us to understand how ecological opportunity and morphological innovation open new adaptive zones and promote radiation, but also opens up future research avenues, such as phylogenetic genome-wide association studies to identify genomic regions under selection during adaptation to aridity; these studies will, in turn, prove invaluable for predicting the effects of climate change on populations and species. Understanding what factors drive speciation in the arid and semi-arid mountains of the biodiversity hotspots of Eurasia allows us to identify areas that possess high diversifying potential, as well as underlying evolutionary processes, which will improve the conservation of biodiversity reserves and their underlying processes. RadiPhyte addresses a timely issue for European science when biodiversity of both the Mediterranean and the Irano-Turanian mountains are especially threatened by climate change. RadiPhyte aims at raising awareness of the global importance of arid mountain biodiversity, in line with the Sustainable Mountain Development of the United Nations. RadiPhyte is also in line with the “Climate change action in developing countries with fragile mountainous ecosystems from a sub-regional perspective” of the EU. We soon aim at sharing the results of RadiPhyte about the continental arid mountains of West and Central Asia with both Austria and Switzerland, countries that are actively involved in major mountain biodiversity programs. Furthermore, Dianthus is the second most important cut-flower crop in the World (generating a trade volume of several hundred million Euros per year) and a well-known and attractive genus. As for any crop, better knowledge of the wild relatives will allow to further crop improvement, a matter especially relevant for developing countries in Eurasia. Dianthus is therefore the charismatic plant needed to rally conservation efforts and awareness in Mediterranean countries, the Middle East, and Central Asia, where nature conservation is a rising priority among the public.