Adaptive radiations of New World lupins revealed by transcriptome sequencing

Lead Research Organisation: University of Oxford
Department Name: Plant Sciences

Abstract

Studies of adaptive radiations - groups of closely related species adapted to very different conditions - have yielded important insights into our understanding of evolution ever since the pioneering works of Darwin and Wallace. Rapid recent radiations of species can be used as models allowing us to study general evolutionary processes that were at work during the major adaptive radiations in the history of our planet. The conditions under which adaptive radiations occur are not well understood and generally it is not clear why some groups of organisms are very species-rich, while others consist of only few species despite similar age. Adaptive radiations can form in a very short period of time, e.g. species-rich groups of African cichlids are only few thousand years old and speciation rates in such groups is very high, yet general reasons for such rapid ('explosive') speciation require further investigation.
This project is devoted to the analysis of evolutionary genetic processes during multiple rapid radiations in a plant genus Lupinus (Leguminosae), which exhibits some of the highest known rates of net diversification in plants. Exceptional rates of species diversification have been documented for Andean lupins, where 85 species have evolved in the last 1.8 million years. An independent lineage of lupins is actively radiating in North America. Such replicate radiations provide powerful comparative systems to address questions about the evolutionary forces driving episodes of diversification. Detailed evolutionary genetic analysis of replicate rapid radiations has not been undertaken previously.
Despite relatively low sequence divergence among recently diverged species of Western New World lupins, the range of life forms (from dwarf annuals and prostrate herbs to small trees), and habitats occupied is striking. This accelerated morphological and ecological diversification suggests that many genes may have been under strong adaptive selection. The aim of the project is to address currently unanswered questions about the types of genes involved in adaptation during adaptive radiations as well as the relative roles of selection at the amino acid level versus regulatory regions. This will involve the comparisons of the patterns of DNA sequence divergence and gene expression between closely related and recently diverged species with divergent life forms and adapted to a range of environments. Genome-wide DNA polymorphism/divergence as well as expression data will be obtained by Solexa/Illumina sequencing of cDNA. This will be done for actively radiating clades of species in the Andes and North America as well as for a set of species outside actively radiating clades for comparison.

Planned Impact

i) Scientific impact:
The question of how do species form and adapt to different and ever changing environments is central to our understanding of biology and evolution. Thus this project has the potential to yield far reaching results and improve our understanding of evolutionary process. Furthermore, it will raise the profile of genus Lupinus as a plant model for adaptation and speciation and will create well resolved phylogeny and genomic (transcriptomic) resources for downstream projects. As a model this genus can rival widely studied and cited African cichlid fishes due to multiple parallel lupin radiations along with nested species diversification rate shifts that coincide with the evolution of derived traits and ecological or geographic shifts. Finally, the proposed research will shed light on the origins of domestication of Andean crop, Lupinus mutabilis in terms of where, when, how many times and from what progenitors this crop was domesticated, knowledge that will contribute to documentation, utilization and conservation of these important crop genetic resources, which is currently obscured by lack of resolution in the phylogeny.

ii) Impact on plant breeding:
Genus Lupinus includes at least four emerging crop species, and one of the species, L. angustifolius, is now an important crop in international trade with exports from Australia alone exceeding 800,000 tonnes per year. Another species, Andean crop L. mutabilis, is the focus of widespread current interest because of its exceptional seed qualities (compares favorably to soyabeans). Morphological and ecological variety of New World (especially Andean) lupins provide a hugely important resource for plant breeding - most species within rapidly diversifying lupin clades can be crossed together, allowing a plant breeder to develop crops for almost any environment. Our project will yield 1) completely resolved phylogenies for rapidly radiating lupin clades and 2) cDNA sequences and gene expression data for a wide set of ecologically and morphologically diverse New World lupins. The phylogeny will help the breeders to choose the right species for breeding programs, while cDNA sequences and gene expression data will be invaluable for identification of genes involved in agriculturally or ornamentally important traits.

iii) Wider public interest:
Evolutionary biology research often enjoys stronger public interest, compared to other areas on biology as it is capable of significantly changing the way we see the world around us. Lupins are a plant group well known by the public due to ubiquitous garden lupin; yet there is little or no awareness of the enormous diversity in this genus. This project will put the garden lupins in the context of genus-wide diversity, providing the public a vivid example of evolution in action.

Publications

10 25 50
 
Description To address the role of adaptation during rapid adaptive radiations we assembled the largest genome-wide dataset including over fifty New World lupin species (including nine not yet formally described species) from rapidly and slowly radiating lineages. The comparison of selective pressures in slowly and rapidly diversifying groups of species revealed massively increased adaptation at both the protein sequence and gene expression levels in the rapidly diversifying clades. We also confirmed this faster adaptation in rapidly radiating clades using comparisons with a number of other plan genera. Our results comprise the first convincing evidence that adaptation plays a significant role during rapid species diversifications. A paper describing these results has been published in Nature Communications in 2016 (doi: 10.1038/ncomms12384).
Furthermore, we used population genetic approaches to analyse the history of speciation in the rapidly diversifying clade of Andean lupins. This analysis revealed that pleistocene glacial cycles have effectively acted as a "species pump" that promoted speciation in this group. The results of this work were published in New Phytologist in 2018 (doi: 10.1111/nph.15243).
Finally, we analysed the origins of the domesticated crop Lupinus mutabilis that is a widely grown oil and protein crop in the Andes. Our demographic analysis demonstrated that this crop is most likely originated from Andean species Lupinus piurensis and domestication of L. mutabilis occured around 1600BC (consistent with sparce archeological findings) and resulted in a major genetic bottleneck (loss of diversity), followed by rapid population growth in the domesticated species. The paper describing these results was published in American Journal of Botany in 2016 (doi: 10.3732/ajb.1600171).
Exploitation Route Our results on adaptive radiations shed light on poorly understood evolutionary processes behind a puzzling fact that some lineages are extremely species rich, while other lineages of similar age are very species poor.
Our results on Lupinus mutabilis domestication help to understand the origins of crops and may have applied interest, as we identify the closest relative of the domesticated crop, which can be used as a source of genetic variation for further crop improvement in breeding.
Sectors Agriculture, Food and Drink,Environment

URL https://www.ncbi.nlm.nih.gov/pubmed/27498896
 
Description John Fell fund small award
Amount £7,500 (GBP)
Organisation University of Oxford 
Sector Academic/University
Country United Kingdom
Start 02/2017 
End 10/2017
 
Description Speciation and adaptation in New World lupins 
Organisation University of Zurich
Country Switzerland 
Sector Academic/University 
PI Contribution This collaboration gives us access to plant material from a vast collection of New World lupins assembled by Dr. Colin Hughes
Collaborator Contribution the collaborator provides plant material
Impact The project is in progress, so we have not yet published anything but are working towards the first paper (hopefully in 2015)
Start Year 2011