The genomic basis of adaptation and species divergence in Senecio

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


This project will exploit the latest developments in DNA sequencing and analysis technologies to study the genomic bases of adaptation and speciation in the plant genus Senecio (ragworts). The principal aim of this work is to determine the relative importance of differences in the coding and regulatory regions of genes in adaptation of species to contrasting environments, our null hypothesis being that these genomic regions contribute equally to adaptation and species divergence. To do this we will compare the nucleotide sequences of protein-coding and regulatory regions of the genomes of Senecio aethnensis and S. chrysanthemifolius, adapted to high and low altitudes, respectively, on Mt. Etna, Sicily, and a hybrid formed between them, S. squalidus (Oxford ragwort), which evolved in Britain following introduction of plants to Oxford from a hybrid zone on Mt. Etna 300 years ago. All 3 Senecio species are adapted to very different habitats and these phenotypic differences will be reflected by genotypic differences detectable by new comparative genomic technologies. Indeed, our previous NERC-funded research has revealed differences in gene expression between the 3 species correlated with phenotypic adaptation. This project will analyse these genetic differences further, and expand genomic comparison through an analysis of the entire gene-rich portion (protein-coding and regulatory sequences) of the genomes of the 3 species. To do this we will establish a partial reference genome by sequencing the gene-space, the non-repetitive fraction of the genome, of Senecio squalidus. This will allow identification of protein-coding and regulatory regions (e.g. promoters and microRNA binding sites). Protein-coding regions of genes can be identified relatively easily using bioinformatic approaches, but identification of regulatory regions requires additional analyses using new technologies designed to identify: i) RNA polymerase- and transcription factor-binding sites (chromatin immunoprecipitation [ChIP-] sequencing), ii) microRNAs (recently discovered ubiquitous gene-regulatory factors) and their binding sites. Once identified, these regions can then be sequenced extensively in multiple individuals of all 3 species to identify differences between them. Evolutionary genetic analysis will then be used to compare patterns of DNA polymorphism to detect 'footprints' of natural selection in protein-coding and regulatory regions that may have been involved in local adaptation and speciation, and also to further investigate the evolutionary history of the 3 Senecio species. In addition, we will investigate changes to promoter binding, DNA methylation (gene silencing) and microRNA expression/targeting between the 3 Senecio species that may be involved in adaptation. Finally, we will test (using plants grown at different UV-regimes) whether altered expression/regulation of candidate genes for local adaptation to high UV light (in high altitude S. aethnensis) is determined by species divergence or phenotypic plasticity. This project will break new ground in evolutionary genomics by being the first to: 1) use functional and evolutionary genetic analyses to analyse the entire gene-space of a plant to detect 'footprints' of selection correlated with adaptation and speciation; 2) explore the role of microRNAs in adaptation and speciation; 3) use large-scale ChIP-sequencing in a plant species. This work will therefore provide unprecedented advances in our current understanding of the role of genomic change in adaptation and speciation.
Description Hybrid zones formed by taxa adapted to contrasting environments represent excellent models to study the genomic bases of adaptation and speciation processes. Adaptation to high and low altitudes in two very closely-related Senecio species on Mt. Etna is a particularly attractive clear-cut case of recent ecological speciation. We used population genetic analysis of DNA polymorphism data to reconstruct the demographic history and selective pressures driving speciation in hybrid zone. We demonstrate that speciation of the high- and low-altitude Senecio species is very recent (Muir et al 2013, Evolution; Chapman et al 2013, MBE) and coincided with the rise of Mt Etna to altitude inhabited by the high-altitude Senecio species (Osborne et al 2013, GBE). Furthermore, we demonstrated that speciation was accompanied by continuous gene flow, refuting the possibility of recent secondary contact and supporting the view that the altitudinal hybrid zone of these Senecio species represents a case of ecological speciation driven by adaptation to contrasting high- and low-altitude conditions (Filatov et al 2016, Molecular Ecology). Finally, we generated a lot of transcriptome and genome sequence data for these non-model organisms and a paper describing the genome and other genomic resources is in preparation.
Exploitation Route This is a basic rather than applied research and our results contribute to better understanding of evolutionary processes that lead to formation of new species.
Sectors Environment

Description Adaptation and speciation in Senecio 
Organisation University of Oxford
Department Mathematical Institute Oxford
Country United Kingdom 
Sector Academic/University 
PI Contribution We generate DNA polymorphism data and conduct evolutionary genetic analyses to infer evolutionary history of closely related Senecio species
Collaborator Contribution The partner provides the knowledge of taxonomy and biology of the species we work with
Impact Chapman MA, Hiscock SJ, Filatov DA. (2016) The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae). J Evol Biol. 29(1):98-113. doi: 10.1111/jeb.12765. Muir G, Osborne OG, Sarasa J, Hiscock SJ, Filatov DA.(2013) Recent ecological selection on regulatory divergence is shaping clinal variation in senecio on Mount Etna. Evolution. 67(10):3032-42. doi: 10.1111/evo.12157. Chapman MA, Hiscock SJ, Filatov DA.(2013) Genomic divergence during speciation driven by adaptation to altitude. Mol Biol Evol. 30(12):2553-67. doi: 10.1093/molbev/mst168. Osborne OG, Batstone TE, Hiscock SJ, Filatov DA.(2013) Rapid speciation with gene flow following the formation of Mt. Etna. Genome Biol Evol. 5(9):1704-15. doi: 10.1093/gbe/evt127.
Start Year 2010