Blackwell Science LtdOxford UKBIJBiological Journal of the Linnean Society0024 4066The Linnean Society of London 2004August 2004 824 453466 Review Article MYTHS AND MECHANISMS B K MABLE Biological Journal of the Linnean Society 2004 82 453 466 With 3 figures 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 that it is too rare to have been a significant factor in animal evolution and its role in plant diversification has been questioned These views have resulted in a bias towards explanations for what deters polyploidy rather than the somewhat more interesting question of the mechanisms by which polyploidy arises and becomes established in both plants and animals The evidence for and against some of the traditional views on polyploidy is reviewed with an attempt to synthesize factors promoting evolution through genome duplication in both groups It is predicted that polyploidy should be more common in temperate than in tropical breeders because environmental fluctuations may promote unreduced gamete formation it should be most common in organisms with sufficient numbers of gametes that random meiotic problems can be overcome and it should be more frequent when mechanisms to promote assortative mating are a direct byproduct of genome duplication 2004 The Linnean Society of London Biological Journal 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 has been strongly biased by discounting of its potential importance in evolutionary diversification by several highly influential researchers In 1925 H J Muller published a paper entitled Why polyploidy is rarer in animals than in plants Muller 1925 that has tended to diminish the value of polyploidy research in animals ever since Although details of the argument have been revisited on occasion Orr 1990 the central dogma that animals should not tolerate polyploidy because of their mode of sexual reproduction has been maintained despite accumulating evidence that many animals do exist as polyploids reviewed in Bogart 1980 Lokki Saura 1980 Schultz 1980 Otto Whitton 2000 Current address Division of Environmental and Evolutionary Biology Graham Kerr Building University of Glasgow Glasgow G12 8QQ UK E mail b mable bio gla ac uk Similarly L G Stebbins in addition to a number of primary papers on the subject wrote two seminal books that have significantly shaped the focus of polyploid research in plants Stebbins 1950 1971 Although Stebbins devoted large sections of each of these books to polyploidy and recognized its wide prevalence in plants he clearly viewed it as a complicating factor that retards rather than promotes progressive evolution so that polyploids are effectively evolutionary dead ends Stebbins surveys of polyploid distributions and patterns have been highly valuable to plant polyploid research but his emphasis on evolutionary limitations has tended to downplay its potential significance By contrast since the late 1960s S Ohno has promoted gene and genome duplication as a significant factor in the evolution of all eukaryotes predominantly based on allozyme data in fish Ohno Wolf Atkin 1968 and predicted that vertebrates have arisen through two rounds of ancient polyploidiza 2004 The Linnean Society of London Biological Journal of the Linnean Society 2004 82 453 466 453 454 B K MABLE tion events in the evolution of fish through to mammals Ohno 1970 1999 Although details of the number and timing of these duplication events remains controversial e g Meyer Schartl 1999 Escriva et al 2002 Page Cotton 2003 Furlong Holland 2004 this issue recent genome analyses have generally supported these early contentions e g Meyer Schartl 1999 Nadeau Sankoff 1997 Spring 1997 Pennisi 2001 Wolfe 2001 Furlong Holland 2004 Although the question of why polyploidy is less frequent in animals than plants is intriguing in its own right the question has been concentrated largely on a limited number of taxa where it is particularly rare predominantly mammals and Drosophila and which are unlikely to reflect the full diversity of animal reproductive strategies This approach has tended to curtail studies of polyploid evolution in animals especially in groups like mammals where the first reports of polyploid species have been made only recently Gallardo et al 1999 2004 this issue A somewhat more fruitful approach for understanding the limits to polyploidization is to ask Why is polyploidy more common in some animal groups than in others and What features do these taxa share with plants that promote evolution through polyploidization Fankhauser 1945 provided a detailed review of the consequences of polyploidy for development in amphibians compared with plants and insects but this type of synthetic approach has not been the focus of many recent studies but see Otto Whitton 2000 The purpose of this paper is to revisit some of the classical views about the evolution of polyploidy in both plants and animals in order to dispel myths that may misdirect research attention and to identify similarities between plant and animal polyploids that could elucidate mechanisms of polyploid origin and establishment in both In the interests of space conservation comparisons will be drawn predominantly between plants and amphibians but similar examples could be drawn from fish e g Mable 2003 Le Comber Smith 2004 this issue or various invertebrate taxa e g Lokki Saura 1980 Adamowicz et al 2002 TRADITIONAL VIEWS CHALLENGING THE MYTHS SEX AND POLYPLOIDY THE DROSOPHILA EYE VIEW Muller s 1925 argument relied on the assumptions that 1 the system of sex determination displayed by Drosophila i e XY male heterogamety in which gender is determined by the ratio of X chromosomes to autosomes in homogametic females represented that found in most animals and that 2 triploids were a necessary intermediate in the formation of evenploidy individuals He suggested that imbalances in sex chromosomes in
View Full Document
Unlocking...