Biological Journal of the Linnean Society , 2004, 82 , 453–466. With 3 figures© 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 453–466 453 Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2004August 2004824453466Review ArticleMYTHS AND MECHANISMSB. K. MABLE *Current address: Division of Environmental and Evolutionary Biology, Graham Kerr Building, University of Glasgow, Glas-gow G12 8QQ, UK. E-mail: [email protected] Biological relevance of polyploidy: ecology to genomics Edited by A. R. Leitch, D. E. Soltis, P. S. Soltis, I. J. Leitch and J. C. Pires ‘Why polyploidy is rarer in animals than in plants’: myths and mechanisms B. K. MABLE* Department of Botany, University of Guelph, Guelph, Ontario, Canada N1G 2W1 Received 20 May 2003; accepted for publication 5 January 2004 Although polyploidy has been involved in speciation in both animals and plants, the general perception is often thatit is too rare to have been a significant factor in animal evolution and its role in plant diversification has been ques-tioned. These views have resulted in a bias towards explanations for what deters polyploidy, rather than the some-what more interesting question of the mechanisms by which polyploidy arises and becomes established in bothplants and animals. The evidence for and against some of the traditional views on polyploidy is reviewed, with anattempt to synthesize factors promoting evolution through genome duplication in both groups. It is predicted thatpolyploidy should be more common in temperate than in tropical breeders because environmental fluctuations maypromote unreduced gamete formation, it should be most common in organisms with sufficient numbers of gametesthat random meiotic problems can be overcome, and it should be more frequent when mechanisms to promote assor-tative mating are a direct byproduct of genome duplication. © 2004 The Linnean Society of London, Biological Jour-nal of the Linnean Society , 2004, 82 , 453–466. ADDITIONAL KEYWORDS: allopolyploidy – amphibians – autopolyploidy – minority cytotype exclusion – multiple origins – sex determination – triploid bridge – unreduced gametes. INTRODUCTION The study of polyploidy in both plants and animals hasbeen strongly biased by discounting of its potentialimportance in evolutionary diversification by severalhighly influential researchers. In 1925, H. J. Mullerpublished a paper entitled ‘Why polyploidy is rarer inanimals than in plants’ (Muller, 1925) that has tendedto diminish the value of polyploidy research in animalsever since. Although details of the argument have beenrevisited on occasion (Orr, 1990), the central dogma thatanimals should not tolerate polyploidy because of theirmode of sexual reproduction has been maintained,despite accumulating evidence that many animals doexist as polyploids (reviewed in Bogart, 1980; Lokki &Saura, 1980; Schultz, 1980; Otto & Whitton, 2000).Similarly, L. G. Stebbins, in addition to a number ofprimary papers on the subject, wrote two seminalbooks that have significantly shaped the focus of poly-ploid research in plants (Stebbins, 1950, 1971).Although Stebbins devoted large sections of each ofthese books to polyploidy and recognized its wide prev-alence in plants, he clearly viewed it as a ‘complicatingfactor’ that ‘retards rather than promotes progressiveevolution’, so that polyploids are effectively evolution-ary dead ends. Stebbins’ surveys of polyploid distribu-tions and patterns have been highly valuable to plantpolyploid research but his emphasis on evolutionarylimitations has tended to downplay its potentialsignificance.By contrast, since the late 1960s, S. Ohno has pro-moted gene and genome duplication as a significantfactor in the evolution of all eukaryotes (predomi-nantly based on allozyme data in fish) (Ohno, Wolf &Atkin, 1968) and predicted that vertebrates havearisen through two rounds of ancient polyploidiza-454 B. K. MABLE © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 453–466 tion events in the evolution of fish through to mam-mals (Ohno, 1970, 1999). Although details of thenumber and timing of these duplication eventsremains controversial (e.g. Meyer & Schartl, 1999;Escriva et al ., 2002; Page & Cotton, 2003; Furlong &Holland, 2004 – this issue), recent genome analyseshave generally supported these early contentions(e.g. Meyer & Schartl, 1999; Nadeau & Sankoff,1997; Spring, 1997; Pennisi, 2001; Wolfe, 2001; Fur-long & Holland, 2004).Although the question of why polyploidy is less fre-quent in animals than plants is intriguing in its ownright, the question has been concentrated largely on alimited number of taxa where it is particularly rare(predominantly mammals and Drosophila ) and whichare unlikely to reflect the full diversity of animalreproductive strategies. This approach has tended tocurtail studies of polyploid evolution in animals, espe-cially in groups like mammals where the first reportsof polyploid species have been made only recently(Gallardo et al ., 1999, 2004 – this issue). A somewhatmore fruitful approach for understanding the limitsto polyploidization is to ask: ‘Why is polyploidymore common in some animal groups than in others?’and ‘What features do these taxa share with plantsthat promote evolution through polyploidization?’Fankhauser (1945) provided a detailed review of theconsequences of polyploidy for development inamphibians compared with plants (and insects) butthis type of synthetic approach has not been the focusof many recent studies (but see Otto & Whitton, 2000).The purpose of this paper is to revisit some of theclassical views about the evolution of polyploidy inboth plants and animals in order to dispel ‘myths’ thatmay misdirect research attention and to identify sim-ilarities between plant and animal polyploids thatcould elucidate mechanisms of polyploid origin andestablishment in both. In the interests of space con-servation, comparisons will be drawn predominantlybetween plants and amphibians but similar examplescould be drawn from fish (e.g. Mable, 2003; Le Comber& Smith, 2004 – this issue) or various invertebratetaxa (e.g. Lokki & Saura, 1980; Adamowicz et al .,2002). TRADITIONAL VIEWS: CHALLENGING THE MYTHSS EX AND POLYPLOIDY : THE D ROSOPHILA EYE VIEW Muller’s (1925) argument
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