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Hybridization and Speciation Richard Abbott, Dirk Albach, Stephen Ansell, Jan Arntzen, Stuart J.E

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Hybridization and Speciation Richard Abbott, Dirk Albach, Stephen Ansell, Jan Arntzen, Stuart J.E International Institute for Tel: +43 2236 807 342 Applied Systems Analysis Fax: +43 2236 71313 Schlossplatz 1 E-mail: [email protected] A-2361 Laxenburg, Austria Web: www.iiasa.ac.at Interim Report IR-13-021 Hybridization and speciation Richard Abbott, Dirk Albach, Stephen Ansell, Jan Arntzen, Stuart J.E. Baird, Nicolas Bierne, Jenny Boughman, Alan Brelsford, C. Alex Buerkle, Richard Buggs, Roger Butlin, Ulf Dieckmann ([email protected]), Fabrice Eroukhmanoff, Andrea Grill, Sara Helms Cahan, Skeie Jo Hermansen, Godfrey Hewitt, Alan G. Hudson, Chris Jiggins, Julia Jones, Barbara Keller, Tobias Marczewski, Jim Mallet, Paloma Martinez-Rodriguez, Markus Möst, Sean Mullen, Richard Nichols, Arne W. Nolte, Cristian Parisod, Karin Pfennig, Amber M. Rice, Michael G. Ritchie, Bernhard Seifert, Carole Smadja, Rike Stelkens, Jacek M. Szymura, Risto Väinölä, Jochen Wolf, Dietmar Zinner Approved by Pavel Kabat Director General and Chief Executive Officer June 2015 Interim Reports on work of the International Institute for Applied Systems Analysis receive only limited review. Views or opinions expressed herein do not necessarily represent those of the Institute, its National Member Organizations, or other organizations supporting the work. doi: 10.1111/j.1420-9101.2012.02599.x TARGET REVIEW Hybridization and speciation* R. ABBOTT1 ,D.ALBACH2 ,S.ANSELL3 ,J.W.ARNTZEN4 ,S.J.E.BAIRD5 ,N.BIERNE6 , J. BOUGHMAN7 ,A.BRELSFORD8 ,C.A.BUERKLE9 ,R.BUGGS10,R.K.BUTLIN11, U. DIECKMANN12,F.EROUKHMANOFF13,A.GRILL14,S.H.CAHAN15,J.S.HERMANSEN13, G. HEWITT16,A.G.HUDSON17,C.JIGGINS18,J.JONES19,B.KELLER20,T. MARCZEWSKI21,J.MALLET22,23,P.MARTINEZ-RODRIGUEZ24,M.MO¨ ST25, S. MULLEN26, R. NICHOLS10,A.W.NOLTE27,C.PARISOD28,K.PFENNIG29,A.M.RICE30,M.G.RITCHIE1 , B. SEIFERT31,C.M.SMADJA32,R.STELKENS33,J.M.SZYMURA34,R.VA¨ INO¨ LA¨ 35, J. B. W. WOLF36 &D.ZINNER37 1School of Biology, University of St Andrews, St Andrews, UK; 2Institute of Biology and Environmental Sciences, Carl von Ossietzky-University Oldenburg, Oldenburg, Germany; 3Natural History Museum, London, UK; 4Netherlands Centre for Biodiversity Naturalis, RA Leiden, The Netherlands; 5CIBIO, Vaira˜o, Portugal; 6Institut des Sciences de l’Evolution, CNRS, Montpellier Cedex 5, France; 7Zoology and BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI, USA; 8Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland; 9Department of Botany, University of Wyoming, Laramie, WY, USA; 10School of Biological and Chemical Sciences, Queen Mary University of London, London, UK; 11Animal and Plant Sciences, The University of Sheffield, Sheffield, UK; 12Evolution and Ecology Program, International Institute for Applied Systems Analysis, Laxenburg, Austria; 13Department of Biology, Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway; 14Department of Tropical Ecology and Animal Biodiversity, University of Vienna, Wien, Austria; 15Department of Biology, University of Vermont, Burlington, VT, USA; 16School of Biological Sciences, University of East Anglia, Norwich, UK; 17Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain; 18Department of Zoology, University of Cambridge, Cambridge, UK; 19Department of Biology, University of Konstanz, Konstanz, Germany; 20Institute of Systematic Botany, University of Zurich, Zurich, Switzerland; 21Royal Botanic Garden Edinburgh, Edinburgh, UK; 22Genetics, Evolution and Environment, UCL, London, UK; 23Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA; 24Department of Biology (Genetics), Universidad Auto´noma de Madrid, Madrid, Spain; 25EAWAG, Du¨ bendorf, Switzerland; 26Department of Biology, Boston University, Boston, MA, USA; 27Max-Planck Institute for Evolutionary Biology, Plo¨n, Germany; 28Laboratory of Evolutionary Botany, Institute of Biology, University of Neuchatel, Neuchatel, Switzerland; 29Department of Biology, University of North Carolina, Chapel Hill, NC, USA; 30Department of Biological Sciences, Lehigh University, Bethlehem, PA, USA; 31Senckenberg Museum of Natural History Goerlitz, Goerlitz, Germany; 32CNRS Institut des Science de l’Evolution, Universite´ Montpellier 2, Montpellier, France; 33Institute of Integrative Biology, University of Liverpool, Liverpool, UK; 34Institute of Zoology, Jagiellonian University, Krako´w, Poland; 35Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland; 36Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden; 37Cognitive Ethology Laboratory, German Primate Center, Go¨ttingen, Germany Abstract Keywords: Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and hybrid species; recombination. It may accelerate speciation via adaptive introgression or cause hybrid zone; near-instantaneous speciation by allopolyploidization. It may have multiple incompatibility; effects at different stages and in different spatial contexts within a single specia- introgression; tion event. We offer a perspective on the context and evolutionary significance of reinforcement; hybridization during speciation, highlighting issues of current interest and debate. reproductive barrier. In secondary contact zones, it is uncertain if barriers to gene flow will be strength- ened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epige- netic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncer- tain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. Correspondence: Roger Butlin, Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK. Tel.: +44 114 2220097; fax: +44 114 2220002; e-mail: r.k.butlin@sheffield.ac.uk *This paper was prepared by the participants of the workshop ‘Hybridization and Speciation’ held at Gregynog Hall, Wales, 23–26 October 2011, and organized by R. K. Butlin, M. G. Ritchie and J. M. Szymura on behalf of the European Science Foundation Network ‘Frontiers in Speciation Research’ (chair: U. Dieckmann). Discussion leaders were: R. Abbott, S. J. E. Baird, N. Bierne, C. A. Buerkle, C. H. Cahan, J. Mallet, A. W. Nolte, C. Parisod and K. Pfennig. ª 2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 229–246 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 229 230 R. ABBOTT ET AL. Introduction debates concerning outcomes of hybridization refer to specific scenarios, it is important to keep this spatial If hybridization is defined as reproduction between and temporal context in mind when considering the members of genetically distinct populations (Barton & broad significance of hybridization. Hewitt, 1985), producing offspring of mixed ancestry, In the context of speciation, hybridization may have then it occurs in almost all proposed processes of several distinct outcomes, which have attracted very speciation. The only exceptions would be cases of com- different levels of research interest. First, there may be pletely allopatric or instantaneous speciation. Hybridiza- a stable, or at least persistent, balance between selec- tion may cause interactions involving a wide range of tion and hybridization, with only some parts of the types and levels of genetic divergence between the genome introgressing between hybridizing populations. parental forms. This divergence may have accumulated This may be true both in tension zones (hybrid zones in different ways including neutral divergence, local involving a balance between selection against hybrids adaptation and coevolution. Any of these may generate and dispersal; Barton & Hewitt, 1985) and in popula- novel phenotypes through interactions in hybrids, tions adapted to distinct habitats (Nosil et al., 2009). including both advantages of transgressive segregation In either case, there may be no progress towards specia- and disadvantages mediated by intrinsic or environ- tion but existing differentiation may be maintained, mentally mediated incompatibilities. Therefore, the with the potential for future divergence when circum- consequences of hybridization and the role it might stances change. Alternatively, barriers to gene exchange play in promoting or retarding speciation can be may breakdown in such a situation, leading to a reduc- expected to vary widely both between different hybrid- tion or loss of differentiation (e.g. Taylor et al., 2006). izing taxa and at different stages of divergence. The opposite type of outcome involves an increase in Hybridization may occur in many different spatial the strength of any barriers to gene exchange and a contexts (Fig. 1). Some of these have been studied progression towards larger areas of the genome being intensively, most notably the formation of hybrid zones protected from introgression (Wu, 2001; Via, 2009). at abrupt parapatric boundaries (Harrison, 1993) and This outcome, where hybridization
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