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UW-Madison BOTANY 940 - Pathways, Mechanisms and Rates of Polyploid Formation in Flowering Plants

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P1: ark/mbg P2: ARS/plb QC: KKK/uks T1: KKKSeptember 28, 1998 10:30 Annual Reviews AR067-17Annu. Rev. Ecol. Syst. 1998. 29:467–501Copyrightc°1998 by Annual Reviews. All rights reservedPATHWAYS, MECHANISMS,AND RATES OF POLYPLOIDFORMATION IN FLOWERINGPLANTSJustin Ramsey and Douglas W. SchemskeDepartment of Botany, University of Washington, Seattle, Washington 98195-5325;e-mail: [email protected]; [email protected] WORDS: polyploidy, autopolyploidy, allopolyploidy, hybridization, speciationABSTRACTPolyploidy is widely acknowledged as a major mechanism of adaptation andspeciation in plants. The stages in polyploid evolution include frequent fertilitybottlenecks and infrequent events such as gametic nonreduction and interspecifichybridization, yet littleis knownabout how these and other factors influence over-all rates of polyploid formation. Here we review the literature regarding polyploidorigins, and quantify parameter values for each of the steps involved in the princi-pal pathways. In contrast to the common claim that triploids are sterile, our resultsindicate that the triploid bridge pathway can contribute significantly to autopoly-ploid formation regardless of the mating system, and to allopolyploid formationin outcrossing taxa. We estimate that the total rate of autotetraploid formation isof the same order as the genic mutation rate (10−5), and that a high frequency ofinterspecific hybridization (0.2% for selfing taxa, 2.7% for outcrossing taxa) isrequired for the rate of tetraploid formation via allopolyploidy to equal that byautopolyploidy. We conclude that the rate of autopolyploid formation may oftenbe higher than the rate of allopolyploid formation. Further progress towardunder-standing polyploid origins requires studies in natural populations that quantify:(a) the frequency of unreduced gametes, (b) the effectiveness of triploid bridgepathways, and (c) the rates of interspecific hybridization.4670066-4162/98/1120-0467$08.00Annu. Rev. Ecol. Syst. 1998.29:467-501. Downloaded from arjournals.annualreviews.orgby University of Wisconsin - Madison on 02/12/07. For personal use only.P1: ark/mbg P2: ARS/plb QC: KKK/uks T1: KKKSeptember 28, 1998 10:30 Annual Reviews AR067-17468 RAMSEY & SCHEMSKEINTRODUCTIONPolyploidy, defined as the possession of three or more complete sets of chromo-somes, is an important feature of chromosome evolution in many eukaryotetaxa. Yeasts, insects, amphibians, reptiles, and fishes are known to containpolyploid forms (100), and recent evidence of extensive gene duplication sug-gests that the mammalian genome has a polyploid origin (112). In plants, poly-ploidy represents a major mechanism of adaptation and speciation (24, 56, 95,104, 120, 157, 159). It is estimated that between 47% and 70% of angiospermspecies are polyploid (56, 110). Differences in ploidy have been observedamong related congeners and even within populations of taxonomic species(24, 34, 56, 100, 156), and there is evidence that individual polyploid taxa mayhave multiple origins (154). These observations suggest that polyploid evolu-tion is an ongoing process and not a rare, macroevolutionary event. Research inagricultural and natural systems indicates that polyploids often possess novelphysiological and life-history characteristics not present in the progenitor cyto-type (95,104). Some of these new attributes may be adaptive, allowing a plantto enter a new ecological niche. Because plants of different ploidies are oftenreproductively isolated bystrong post-zygotic barriers, polyploidy is also one ofthe major mechanisms by which plants evolve reproductive isolation (34, 56).In spite of the prevalence and importance of polyploidy, the factors con-tributing to polyploid evolution are not well understood (165). Two criticalstages of polyploid evolution can be identified: formation and establishment.To understand the process of polyploid formation requires information on thepathways, cytological mechanisms, and rates of polyploid formation. To assessthe likelihood that a new polyploid will successfully establish requires infor-mation on the viability and fertility of new cytotypes, the extent of assortativemating and reproductive isolation within and between different cytotypes, andthe ecological niche of new polyploids. Here we review the literature concern-ing polyploid formation to answer the following questions: (a) What are theprimary pathways and mechanisms of polyploid formation? (b) What are theparameters for each of the steps involved in polyploid formation? (c) Whatare the numerical values reported for these parameters? and (d) What is theestimated rate of polyploid formation by each pathway?One major motivation for this review is to synthesize the diverse litera-ture on polyploid origins and thereby provide a resource for the developmentof future empirical and theoretical studies of polyploid evolution. To thisend, we have tabulated data from many studies and made this informationavailable on the Annual Reviews web site (http://www.annualreviews.org; seeSupplementary Materials). We summarize these data throughout the text andidentify the location of each database on the web site.Annu. Rev. Ecol. Syst. 1998.29:467-501. Downloaded from arjournals.annualreviews.orgby University of Wisconsin - Madison on 02/12/07. For personal use only.P1: ark/mbg P2: ARS/plb QC: KKK/uks T1: KKKSeptember 28, 1998 10:30 Annual Reviews AR067-17POLYPLOID FORMATION 469By necessity, many of the plants considered in this review are agriculturalor horticultural cultivars and their wild relatives, as well as taxa widely usedin classical genetic studies (e.g. Oenothera and Datura). We believe that thestudies reviewed here provide insights into the process of polyploid formationin natural populations, but caution that further research in natural populations isneeded to test our findings. Our survey draws from a wide range of plant taxa,but because of the limited number of studies, we do not interpret our results ina phylogenetic context.In this chapter, 2n refers to the somatic chromosome number and n to thegametic chromosome number regardless of the degree of polyploidy, while x isthe most probable base number. This gives the following cytological designa-tions: diploids (2n = 2x), triploids (2n = 3x), tetraploids (2n = 4x), etc. Indescribing crosses within and between cytotypes, the maternal parent is alwayslisted first.MECHANISMS OF POLYPLOID FORMATIONSeveral cytological mechanisms are


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UW-Madison BOTANY 940 - Pathways, Mechanisms and Rates of Polyploid Formation in Flowering Plants

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