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Durham Research Online Durham Research Online Deposited in DRO: 02 April 2020 Version of attached le: Published Version Peer-review status of attached le: Peer-reviewed Citation for published item: Walter, Greg M. and Abbott, Richard J. and Brennan, Adrian C. and Bridle, Jon R. and Chapman, Mark and Clark, James and Filatov, Dmitry and Nevado, Bruno and Ortiz Barrientos, Daniel and Hiscock, Simon J. (2020) 'Senecio as a model system for integrating studies of genotype, phenotype and tness.', New phytologist., 226 (2). pp. 326-344. Further information on publisher's website: https://doi.org/10.1111/nph.16434 Publisher's copyright statement: c 2020 The Authors. Additional information: Use policy The full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for personal research or study, educational, or not-for-prot purposes provided that: • a full bibliographic reference is made to the original source • a link is made to the metadata record in DRO • the full-text is not changed in any way The full-text must not be sold in any format or medium without the formal permission of the copyright holders. Please consult the full DRO policy for further details. Durham University Library, Stockton Road, Durham DH1 3LY, United Kingdom Tel : +44 (0)191 334 3042 | Fax : +44 (0)191 334 2971 https://dro.dur.ac.uk Review Tansley review Senecio as a model system for integrating studies of genotype, phenotype and fitness Authors for correspondence: Greg M. Walter1 , Richard J. Abbott2 , Adrian C. Brennan3 , Greg M. Walter 1 4 5 5 Tel: +44 (0)7305 866305 Jon R. Bridle , Mark Chapman , James Clark , Dmitry Filatov , Email: [email protected] Bruno Nevado5 , Daniel Ortiz-Barrientos6 and Simon J. Hiscock5 1School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, UK; 2School of Biology, University of St Andrews, St Andrews, Simon J. Hiscock Tel: +44 (0)1865 610302 Fife, KY16 9TH, UK; 3School of Biological and Biomedical Sciences, University of Durham, Durham, DH1 3LE, UK; 4School of Email: [email protected] Biological Sciences, University of Southampton, Southampton, SO17 1BJ, UK; 5Department of Plant Sciences, University of Oxford, Received: 19 July 2019 Oxford, OX1 3RB, UK; 6School of Biological Sciences, University of Queensland, St Lucia, QLD 4072, Australia Accepted: 17 December 2019 Contents Summary 326 VI. Genomics of adaptation and speciation 337 I. Model systems for experimental ecology and evolution 326 VII. Integrating studies of genotype, phenotype, and fitness 338 II. Senecio as an experimental model system 327 VIII. Conspectus 340 III. Mating system diversity and evolution in Senecio 329 Acknowledgements 340 IV. Mechanisms and consequences of hybrid speciation 334 References 340 V. Adaptation and speciation in Senecio 335 Summary New Phytologist (2020) 226: 326–344 Two major developments have made it possible to use examples of ecological radiations as model doi: 10.1111/nph.16434 systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype, and Key words: adaptive radiation, Asteraceae, fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for genomics, hybrid speciation, model system, integrating field and laboratory experiments with detailed genetic sequencing. Combining these quantitative genetics, self-incompatibility, approaches allows evolutionary biologists to better study the interplay between genotype, Senecio. phenotype, and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories, and morphologies, and they occupy a multitude of environments. Common within the genus are species that have hybridized naturally, undergone polyploidization, and colonized diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology. I. Model systems for experimental ecology and organisms, providing important insights into genome evolution, the structure of developmental pathways, and the control of gene evolution expression. However, to answer fundamental questions in ecology Recent technological advances in genomic and computational and evolutionary biology we need to develop model systems that technologies have allowed genetic analyses of many nonmodel integrate these novel genetic resources with experimentally flexible 326 New Phytologist (2020) 226: 326–344 Ó 2020 The Authors www.newphytologist.com New Phytologist Ó 2020 New Phytologist Trust New Phytologist Tansley review Review 327 systems that are also ecologically diverse. Using ecologically different environments (Wu et al., 2008), but Senecio has the divergent systems is critical for understanding how genotypes added benefit of a world-wide distribution, and a greater relate to phenotypes across different environments, and to test the diversity of species that include a range of mating systems and a processes driving adaptation, speciation, and biogeographical multitude of growth forms (Fig. 1). Such diversity in morphol- patterns. Nevertheless, many model systems used in evolutionary ogy and habitat makes Senecio attractive to a similar diversity of biology are only studied in laboratory settings because, despite scientists, from ecologists to phylogeneticists, molecular geneti- possessing key experimental attributes (e.g. short life cycles, self- cists, and quantitative geneticists. We therefore propose Senecio fertility), they show limited variation in life history, mating system, as an attractive model system for answering fundamental or habitat. The utility of such systems for detailed laboratory or questions in ecology and evolution, joining the ranks of glasshouse experiments therefore limits their value in field Antirrhinum, Arabidopsis (including Boechera and other rela- experiments testing hypotheses relating to evolution and ecology, tives), Helianthus, Mimulus, Silene,andSolanum. such as the interaction between phenotypic plasticity and natural selection, and how and when populations specialize to particular 1. What questions can we answer using Senecio? environments. This limitation has become increasingly relevant given the urgent need to predict how, where, and how quickly Future work will benefit from the imminent completion of high populations and ecological communities will respond to ongoing coverage and highly contiguous annotated genomes for Senecio environmental change. Research needs to focus on model systems squalidus and Senecio lautus (B. Nevado et al., unpublished; with populations and species that inhabit different environments Wilkinson et al., 2019). These will be used as references for further and ecosystems, but which remain amenable to large field genomic analyses of other Senecio species, including whole-genome experiments and quantitative genetic crossing designs. Specifically, resequencing, DNA methylation, and RNA sequencing (RNA-seq) we need model systems that can connect genotype, phenotype, and approaches. These new resources will make Senecio a powerful fitness under a range of environmental conditions. In this review, system to study the genomic architecture of selection, adaptation, we argue that Senecio is one of very few model systems that can fill and divergence across environments. Combining such genetic this role. association techniques with quantitative genetic crossing designs is a powerful way to explore how the relationship between genotype, II. Senecio as an experimental model system phenotype, and fitness changes across environments. Of special importance is the ease and speed at which species of Senecio can be Senecio (Linnaeus, 1753) is a large genus of flowering plants propagated from cuttings. This ability to generate clones allows within the tribe Senecioneae of the daisy family, Asteraceae. researchers to control for genotype and transplant large numbers of Containing in excess of 1200 species distributed across the globe, clones across multiple environments, setting Senecio apart from Senecio radiated rapidly during the Miocene c. 10.7 Ma to other model systems. Such approaches can address an array of become one of the largest genera of flowering plants (Kandziora questions in ecology, evolution, and evolutionary genomics (see et al., 2017). Species of Senecio, commonly known as ragworts Box 1). and groundsels, are generally herbaceous, but also occur as vines, shrubs, succulents, epiphytes, and small trees (Fig. 1). The genus 2. Origins and diversity of Senecio is aptly named after the tendency for species to produce senescent flower heads resembling tufts of white hair (Latin The presence of repeated radiations in the Americas, Australasia, ‘senex’ = ‘old man’) formed by the pappus, which facilitate and across northern Africa into Europe highlights the ability of airborne seed dispersal. Senecio to colonize and rapidly adapt to multiple environments Many species of Senecio have useful attributes of a model (Comes & Abbott, 2001;
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