| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Book Review |
Department of Botany, University of Guelph, Guelph, Ontario, N1G 2W1 Canada
Chromosomal variation is widespread in plants and animals. It often contributes to the genetic barriers to gene flow that exist between species and hence its role in species diversification has been heavily debated (White, 1978
; King, 1993
; Rieseberg, 2001
). The potential importance of plant genetic systems as arbiters of gene transmission and species diversification was recognized early in the 20th century by Darlington (1939)
, Huxley (1942)
, and, most recently, by Stebbins, in his 1971
book Chromosomal Evolution in Plants. Since that time, our understanding of these phenomena has progressed considerably as a result of theoretical research on hybridization and genome duplication and technical advances in PCR, chromosomal painting, genetic mapping, phylogenetic analyses, and flow cytometry. But as King (1993
, p. 3) stated, "despite the body of new and exciting cytogenetic, biochemical and molecular data, numerous recently published books or conference proceedings have either downgraded the significance of chromosomal speciation, or simply ignored it in favor of speciation by genetic differentiation." With over 30 years since the last synopsis in plants, Levin's book on chromosomal evolution is therefore timely and welcome.
Levin is a prominent researcher in plant evolutionary biology. He recently published another book in the Oxford Series (Levin, 2000
) and is well qualified to review the field of chromosomal evolution in plants. Based on the book's Preface, Levin's intent is to provide a ‘...contemporary synthesis’ of plant evolution associated with chromosomal rearrangements such as translocations, inversions, fissions, fusions, and genome duplications. The text is geared towards ‘students or professionals’ and, importantly, the overarching goals are to integrate the ‘fragmented’ literature on chromosomal diversity and to place this body of research within a speciation context. Chapters are devoted to variation in genome size, chromosomal rearrangements, aneuploidy, barriers to gene exchange, permanent translocation heterozygotes, and polyploidy. The topics are not dealt with uniformly, with polyploidy occupying four of the nine chapters and permanent translocation heterozygosity, a relatively rare phenomenon, given an entire chapter. In each chapter, Levin describes the current state of research, outlining the major issues and providing examples to illustrate recent results. Here I summarize the major topics in the book and evaluate the effectiveness with which they are presented. As I point out below, the book will be useful as a general reference, especially for students, but its primary weakness is in the lack of integration among topics and synthesis with the speciation literature.
One aspect of plant genetic systems that has received little attention in other books on chromosomal change is genome size. Plants exhibit remarkable variation in this trait and, although its role in speciation has not been explicitly considered, the proximate and ultimate causes have been debated by evolutionists for over 20 years. At the center of this controversy is whether genome mass has adaptive value or whether it is simply an incidental byproduct of the accumulation of noncoding DNA ("Junk DNA Hypothesis"). Most of the recent developments in this field have resulted from technical rather than conceptual advances. Chapter 1, "Heterogeneity in Genome Size," provides a good review of our progress in plants and evaluates them in relation to functional and nonfunctional evolutionary hypotheses. For example, flow cytometry and micro-densitometry have permitted more precise and rapid estimates of genome size compared to the historical practice of using chromosome length. The contemporary approaches have revealed much variation within as well as between species, including fine scale correlations with geography, development rate, and morphology. In addition, molecular approaches have provided phylogenetic information with which to evaluate the directions and rates of genome size evolution and have enabled a better understanding of the role of repetitive DNA as the basis for these size increments. Overall, the material in this chapter is clearly presented and points unmistakably in favor of an adaptive role for genome size in plant evolution. Less well developed, however, are the more mechanistic questions such as "What is the basis for genetic instability in genome size?" "What is the adaptive significance of variation in genome size among tissues of single individuals (endopolyploidy)?" and, "Why does average genome size drop with increasing ploidy?"
As an aside, there is confusion in the literature regarding terms such as genome size and C value. In a strict sense, genome size refers to the mass of a single chromosome complement, whereas 1C and 2C values refer to the DNA content of gametic and somatic tissues, respectively. This distinction is particularly important in polyploids because the 1C value will necessarily contain more than one genome copy. Therefore, reliable estimates of genome size require information about the organism's ploidy, not to mention appropriate standards, replication, and environmental controls when using techniques that rely on DNA-specific dyes. Unfortunately, many researchers fail to appreciate the distinction of terms and Levin's brief introductory paragraph does little to identify or ameliorate the problem. The confusion is further exacerbated, through no fault of Levin's, by having to continuously switch from one measure to another when reviewing examples from the literature. This inconsistency in measurement and reporting may be unavoidable in some cases, but may lead to some confusion in building large global databases.
Chapters 2 through 5 deal with various kinds of chromosomal rearrangements, such as translocations, inversions, fissions, and fusions. In general, this section is full of useful information. My overall concern is with the style of presentation and the lack of a prominent evolutionary context throughout. The material is offered in a highly descriptive way, listing topic after topic and, within each, providing an extensive list of examples to illustrate the breadth of results. A concerted effort to synthesize the literature and place it in the context of current speciation models as well as to discuss future research would have increased the value and level of interest for both student and researcher.
Chapter 2, "Chromosomal Rearrangements," focuses on the two most common forms of rearrangement: translocations and inversions. It begins by describing the recognizable chromosomal rings, bridges, and fragments at meiosis that are characteristic of such chromosomal variants. As the primary basis for identifying most rearrangements these meiotic signatures provide a useful starting point and probably deserve more than one slightly fragmented paragraph for review. The chapter then describes the frequency and distribution of translocations and chromosomal inversions in flowering plants. Here, the examples are all useful but begin to resemble an endless list with little glue to tie them together.
What is most puzzling from an evolutionary perspective is why there is so much heterogeneity in the incidence of rearrangements and how novel cytotypes become fixed in new species. These questions are central to the debate over whether rearrangements play a causative or an incidental role in speciation and can best be addressed by considering the factors influencing both the formation and the establishment of novel rearrangements in populations. While Levin does not follow this division explicitly (as he does in Chapter 6 on polyploids), he does touch on a few of the relevant issues. He points out that the formation of new rearrangements is likely governed by factors influencing spontaneous chromosome breakage, and emphasizes how little we know about what causes breakage, and, in fact, there "...have been no direct measures of spontaneous breakage rates." This represents a critical void in our understanding, and without this information we will never fully understand the dynamics of chromosomal variants in natural populations.
The establishment and fixation of novel rearrangements is equally important and is an issue of considerable debate. In general, establishment is viewed as extremely unlikely because of the low fitness of most rearrangements when in a heterozygous form. This scenario equates with an under-dominance model in population genetics, under which fixation of rare chromosomal variants is very unlikely due to strong positive frequency-dependent selection. Despite the importance of this line of questioning to speciation, Levin devotes a mere 2.5 pages to this problem and neglects much of the relevant literature on this topic, including several theoretical models that propose evolutionary scenarios for overcoming the obstacle of under-dominance (King, 1993
; Rieseberg, 2001
) and relevant empirical tests of these ideas. Inbreeding was offered as one selective force favoring translocation heterozygotes, but this is likely insufficient to overcome the overall lower fitness of heterozygotes. To his credit, Levin does discuss the role of drift in fixing novel chromosomal variants. However he spends an inordinate amount of time describing the subtleties of effective population size, rather than evaluating the empirical evidence (or lack thereof) for stochastic forces in chromosomal evolution.
Plant evolution via aneuploidy, or changes in chromosome number due to rearrangements, is vastly understudied and, relative to its prevalence, has an undeservedly low profile compared to polyploidy. This is the primary theme for Chapter 3. Unfortunately, I found it to comprise a collection of rather disparate topics, many with no obvious relation to aneuploidy. Two aspects of aneuploid chromosomal variation are discussed, albeit in different locations: the cytogenetic mechanisms of aneuploid changes and aneuploid series in different plant groups. The causes of aneuploid chromosome changes are only briefly outlined and the description is not clear nor is it sufficient to explain the accompanying figure. The section on aneuploid series uses several examples to demonstrate that chromosome changes can be quite extensive in some taxa and that it occurs primarily through the progressive loss of chromosomes. These results are even more interesting in that they can occur in association with shifts in life history and incidence of asexual reproduction (e.g., apomixis). However, nowhere in this chapter does Levin consider the ecological or genetic factors driving the formation or establishment of aneuploid variants, nor the theoretical difficulties associated with how aneuploid variants are fixed in populations. The only discussion on speciation is a brief review of aneuploid races but, oddly enough, this is located in the chapter on chromosomal rearrangements.
The remaining topics in this chapter do not fit with the aneuploid theme and have the appearance of being placed here because they do not fit anywhere else. To begin, Levin provides a general description of typical karyotype analyses. This is valuable, especially in providing a historical context to studies in chromosomal evolution. Without doubt, such a fundamental topic deserves to be in the book, but perhaps in an introductory chapter that defines different aspects of the genetic system of plants. The chapter goes on to describe various data on karyotype diversity, including chromosome asymmetry and size, which have no direct relevance to aneuploidy. Equally confusing is the presence of a section on molecular cytogenetics and chromosomal evolution. Genetic mapping and chromosome painting have been instrumental in providing markers for understanding the nature of chromosomal differences among taxa and also are deserving of much attention; however, the discussion here has more to do with chromosomal asymmetries and rearrangements than aneuploidy. As a result of being out of context, the value of these contemporary approaches may be underappreciated or lost on the reader.
Up to and including the third chapter, the book does an admirable job of describing variation in chromosomal characteristics, but offers few insights into the implications for speciation. Chapter 4 is the only chapter that addresses this issue directly by considering the impact of chromosomal rearrangements as post-mating isolating mechanisms. Devoting a single chapter to this makes sense, given that the evolutionary forces at play are similar (with some exceptions) regardless of the kind of chromosomal rearrangement. The contribution of chromosomal changes to reduced gene flow between species occurs via two known mechanisms: low fertility in hybrids and reduced recombination rates. It has long been recognized that chromosomal differences among taxa can lead to reduced fertility in hybrids as a result of mispairing and malsegregation of chromosomes at meiosis. Levin makes this point convincingly and also shows that fertility can vary depending on the number of chromosomal differences. However, less effort was devoted to what is not known. Most notably, we have little knowledge of the ecology of rearrangement homozygotes and heterozygotes. In particular, information regarding their growth and viability, mating relationships, and eco-geographic differentiation are essential for understanding the effects of rearrangements on fitness (not just fertility) and assessing the likelihood that rare chromosomal variants will spread to fixation.
Hybrid sterility is not the only avenue by which different chromosomal species may be isolated. In fact, fertility effects can be unpredictable, incomplete, or even absent for some chromosomal variants (e.g., for differences in heterochromatin) and for certain mechanisms of segregation (Coyne et al., 1993
; Rieseberg, 2001
). In these cases, hybrids can produce gametes of variable quality that may impact the dynamics of chromosomal variants in populations and hence the probability of fixing a novel variant. Because sterility is less predictable than first thought, Rieseberg (2001)
has argued that the most important impact of chromosomal rearrangements on isolation may be through their effects on recombination. Theoretical models show that gene flow near under-dominant loci will decline in proportion to the hybrid fitness disadvantage. Similarly, recombination rates are expected to be lower in rearranged segments of chromosomes. Rieseberg's empirical studies of introgression between two species of Helianthus now confirm this and suggest that rearrangements of large effect may suppress gene flow across extensive chromosomal segments.
The effects of chromosomal rearrangements on reproductive isolation are central to any discussion on speciation. But this issue alone does not adequately reflect the many dimensions of this issue and specifically the question of whether chromosomal variants are the basis for species divergence. Unfortunately, this controversy is never dealt with in this or any other chapter. As mentioned previously, the major opposition to a role for chromosomal speciation is that it is theoretically difficult for a novel variant to be fixed except in small, inbred populations. However, and at the risk of repeating myself, there are a number of models that have examined factors that might overcome this barrier, such as geographic isolation, meiotic drive, accumulation of multiple rearrangements, and ecological differentiation among chromosomal variants (reviewed in King, 1993
; Rieseberg, 2001
). Moreover, the significance of recurrent mutations, selfing, or the magnitude of pre-zygotic isolation associated with chromosomal variation has not been examined but may facilitate speciation by weakening the impact of selection against rare cytotypes and simultaneously maintaining strong reproductive isolation. In this book, no attention is paid to these counter proposals or to general arguments for or against chromosomal speciation. This is surprising given Levin's many valuable contributions to our understanding of population processes underlying plant evolution.
No book on chromosomal evolution in plants would be complete without mention of permanent translocation heterozygosity, and Levin devotes the fifth chapter to this subject. Here, he describes its taxonomic distribution, evolutionary dynamics, genetic consequences, and provides a brief discussion of how such heterozygotes may arise in the first place. For the latter question, he describes two major pathways, one involving ‘...the gradual accumulation of translocations in outcrossing populations undergoing severe inbreeding’ and the other, ‘...hybridization between chromosomally divergent races or species.’ Other than species whose members differ in the number of translocations they carry, the evidence for the former mechanism seems sparse. Moreover, assuming that early translocations result in reduced fertility in hybrids, it is unclear how they would persist long enough to support an accumulation of them. In the second pathway, more explanation of the population process and the significance of self-incompatibility would be useful for a clearer description of these hypotheses. Most important, it is clear that the full force of contemporary molecular tools have not been brought to bear on this topic and therefore this section would have benefited from a more general discussion of the opportunities for future work.
Chapters 6 through 9 examine various aspects of polyploidy, the multiplication of whole chromosome sets. Although estimates vary, this phenomenon represents one of the single most common evolutionary changes in the genetic system of plants (aneuploidy not included), and many prominent biologists refer to it as one of few mechanisms of instantaneous, sympatric speciation (Mayr, 1942
). Like other chromosomal variants, however, the jury is still out with respect to its contribution to species diversification. As Levin points out, our current estimates of polyploidy are likely low, as molecular-based phylogenies and genetic maps reveal that polyploid taxa are often polyphyletic, and that many species, previously viewed as diploid, are likely ancient polyploids. In contrast, the absence of surveys conducted in a phylogenetic context may mean that the number of independent origins of polyploids is overestimated. Despite its prevalence, there are virtually no estimates of the proportion of speciation events associated with polyploidy (although see Otto and Whitton, 2000
) and no comprehensive analyses of the process by which polyploids form and spread in populations of their diploid progenitors (Thompson and Lumaret, 1992
). While Levin attempts to summarize research in these areas, he never really identifies the current voids nor does he relate them to conventional views of polyploid speciation.
Chapter 6 is devoted to the evolutionary dynamics of polyploidy. It begins with a review of the pathways of polyploid evolution. As Levin describes, the union of unreduced gametes (n = 2n) is considered the prime mechanism of polyploid formation. Ironically, the evidence for this is minimal. Yes, unreduced gametes (both sperm and eggs) are frequently produced by diploid plants and variation in unreduced gamete formation has a large genetic and environmental component. However, most of our knowledge comes from crop plants, whereas the magnitude and role of unreduced gametes in natural populations is largely unexplored. Moreover, the discrepancies between the frequency of unreduced gametes and the number of polyploid offspring produced in controlled crosses highlights the danger in equating the existence of a potential mechanism with its relative importance in the field. Repeating the same flaw in logic, Levin evaluates the role of unilateral polyploidization through the triploid bridge by examining the causes for abortion of triploid offspring. I have yet to read a clear explanation for the Endosperm Balance Number (EBN) in a reference book or review, and this was no exception. More problematic, by dwelling strictly on causes of triploid block, Levin masks the fact that triploids are often partially viable and fertile (Ramsey and Schemske, 1998
) and can play an important role as intermediaries in tetraploid formation (triploid bridge). Indeed, recent studies suggest that triploids appear in a surprising number of polyploidy taxa and that their contribution can be significant even when their fitnesses are low (Felber and Bever, 1997
; Husband, in press
). However, with relatively little empirical research in this area, our knowledge of the rates and pathways of polyploidy formation in the wild remains largely theoretical. Flow cytometry will hopefully provide some hope by offering a means of detecting and sorting unreduced gametes in natural populations and for quantifying rates of triploid production. In addition, highly variable markers such as microsatellites will be needed to trace the origins of tetraploid offspring and to distinguish bilateral polyploidization (2x x 2x crosses) from the triploid bridge. To date, this has not been done.
Compared to research on chromosomal rearrangements, researchers have made some inroads into the evolutionary forces governing the establishment of polyploids, in part due to Levin's own contributions to this field. Levin laid the foundation by demonstrating the theoretical barriers to tetraploid establishment as a result of the low fitness of triploids and a frequency-dependent mating disadvantage (Minority Cytotype Exclusion Levin, 1975
). This has stimulated numerous empirical and further theoretical studies of ecological and genetic factors that may overcome this barrier, including assortative mating, competitive ability, ecological differentiation, and unreduced gamete production. However, research on these topics is limited to a few model systems and little work has been done to relate them, individually or collectively, directly to polyploid establishment in natural populations. Studies of assortative mating exemplify this very well. Numerous studies of flowering asynchrony between ploidy levels have demonstrated partial reproductive isolation, and a few studies on pollinator fidelity suggest the same. However, there are no comprehensive studies of the reproductive barriers between diploids and tetraploids that investigate the relative importance of pre- vs. post-zygotic mechanisms or their combined effects on polyploid establishment. Moreover, Levin suggests that assortative mating will ‘...promote tetraploid invasibility’; however, recent models, including one of his own, suggest this is not always the case. In other words, more work is required to understand both the theoretical impacts of these processes as well as their relative contributions in natural populations. In addition to the factors already mentioned that may affect establishment, Levin introduces an additional ecological mechanism, specifically that polyploidy can become established through the colonization of new habitats, rather than spreading in diploid populations. Coupled with ecological differentiation this metapopulation process may be one of the most important and yet most neglected factors aiding polyploid speciation.
Toward the end of Chapter 6, Levin describes the eco-geographical patterns of diploids and polyploids. Using a plethora of examples, he convinces us that differences in distribution exist between ploidy levels. While I am not disputing this, I think a more critical analysis would have determined that geographic separation does not necessarily imply ecological differentiation and that many of the generalities derived from this data have been based on comparative studies that do not account for phylogeny. Therefore, the existing data provides a weak test of hypotheses about the association between polyploidy and either breadth of ecological tolerance or predisposition to harsh, disturbed, or cold environments. Similarly, in the discussion of contact zones between diploids and polyploids, Levin does not make the distinction between environmentally dependent and independent mechanisms for maintaining hybrid zones. This reflects the confusion in the polyploidy literature regarding the influence of ecological differentiation vs historical colonization patterns in molding ploidy structure. Unfortunately, most molecular approaches on polyploid systems have not had a strong phylogeographic focus, which is necessary to identify primary and secondary contact zones. Even more surprising, there is not a single published study in which diploids and polyploids have been transplanted reciprocally as a method of distinguishing between adaptive and historical processes.
In Chapter 7, Levin describes the many physiological, morphological, and ecological differences between polyploids and diploids. This question is important for understanding the adaptive significance of polyploidy. In general, the chapter is a thorough analysis of a variety of traits but there is no obvious attempt to synthesize or critically evaluate this data. Clearly, we need to understand whether chromosome multiplication can influence phenotypes. However, to make progress, we must develop the ability to predict these phenotypic shifts and to understand their underlying genetic causes. To achieve this, we need studies that relate synthesized polyploids to the characteristics of their diploid progenitors. In addition, inserting candidate genes into polyploids in varying copy number may help to separate the effects of gene dosage from the nucleotypic effects of polyploidy. Part of the problem to date is that most studies of noncrop species involve comparisons of extant diploids and tetraploids. These studies are plagued by the fact that it is impossible to distinguish the effects of chromosome doubling from the effects of selection operating subsequent to the doubling event. Synthetic polyploids will be essential for this but have not been emphasized enough in this chapter.
Molecular markers have revamped our understanding of plant evolution through polyploidy in many ways. As Levin suggests, protein and DNA polymorphisms have provided valuable tools for detecting polyploid variation and for discriminating between those derived from within a single species (autopolyploid) and those from hybridization between species (allopolyploid). Historically, autopolyploids have been regarded as relatively rare perhaps because of the close morphological resemblance between autopolyploids and their diploid progenitors and due to the complex and varying cytogenetic criteria on which their definitions are based. Indeed, the rising count of autopolyploids as a result of molecular studies confirms that the dominance of allopolyploids may be as much a detection problem as anything. An additional result from marker-based approaches has been the growing evidence for the multiple origins of many polyploid taxa, both auto- and allopolyploid. Recurrent origins provide an explanation for the high variability within polyploid lineages, summarized by Levin in Chapter 8. This pattern also suggests that polyploid evolution is more dynamic than once believed and thus is amenable to population approaches, which are described in Chapter 6. However, closer inspection reveals that many of these evolutionary studies are not based on genealogical relationships among ploidies. Moreover, it is becoming obvious that diploids and polyploids can and do exchange genes, albeit infrequently, after secondary contact. Therefore I agree with Levin that the onus will be on researchers to make use of phylogenetic and geographic data to discriminate more rigorously between single and polyphyletic origins, secondary and primary contact zones and to identify localized origins of polyploids from genetically distinct diploid populations.
In describing the changes in genome structure and expression that occur immediately after formation of allopolyploids, Levin saves one of the most exciting areas in polyploid research until the end. As Levin mentions, the "...conventional wisdom held that allopolyploids contained distinct genomes ... that remain independent entities." However, research using genomic in situ hybridization (GISH), genetic linkage maps, and expression studies show that extensive within-genome rearrangements, gene silencing, and inter-genome translocations can occur, many within the first few generations following their synthesis (Soltis and Soltis, 2000
, Ozkan et al., 2001
; Adams et al., 2003
). The use of synthetic polyploids for studying these processes has elevated polyploid research to the realm of experimental evolution and is changing our perceptions of polyploids as evolutionary dead-ends. The exciting insights that are being discovered, however, represent only the beginning of this new field. Hopefully, synthetic polyploids will also provide a window on the rapid evolutionary divergence of phenotypic traits that are of significance to adaptation and speciation.
In summary, then, this book is a valuable source of information on many different aspects of chromosomal variation in plants. It is heavily referenced, comprehensive, and is well worth having on the shelf. The book was reasonably well written, although there were a moderate number of typographical errors throughout, and whole paragraphs were repeated in more than one section. Despite this, I found the writing relatively easy to follow, with the exception of some critical concepts (e.g., genome size, EBN) and cytogenetic properties (synaptonemal complex, fission, fusion), which required more complete explanations. As mentioned before, entire sections of some chapters seemed out of place, making the logic difficult to follow at times. The large number of examples used throughout the book ordinarily would be an asset; however, I would have given some up in place of more synthesis, both within individual topics and in the context of speciation. Finally, more time devoted to future research might have done more to build bridges between the various subdisciplines and would have made the volume more forward-looking and influential on future research.
One thing this book highlighted for me was how research on polyploid and non-polyploid chromosomal evolution have operated as two solitudes. It is surprising to me how many common theoretical issues (e.g., under-dominance, minority cytotype disadvantage, hybrid infertility) lie at the heart of these two fields, especially as they pertain to speciation, and yet how insular they have been. That being said, the structure of this book was not completely conducive to achieving such integration and thus missed a valuable opportunity. For example, having chapters on individual chromosomal variants is understandable but it encourages the traditional focus on specific phenomena rather than on evolutionary processes to which they contribute, such as reproductive isolation, evolutionary dynamics, and speciation. To be fair, Levin attempted to draw parallels between the evolutionary dynamics of polyploids and chromosomal translocations. Unfortunately it was very brief and buried within a section in Chapter 6. At the very least, the book would have benefited from a short introductory chapter that outlines the basic components of the karyotype and the historical role of chromosomal mechanisms of speciation. In addition, a synthesis at or near the end would have provided a bookend to reinforce the major evolutionary themes and to make much-needed comparisons among the different kinds of chromosomal variation. The lack of integration among theoretical and empirical research on different kinds of rearrangements reminds us how much work lies ahead before we can understand with any certainty the role of chromosomal mechanisms in plant speciation.
 |
FOOTNOTES |
|---|
2 E-mail: bhusband{at}uoguelph.ca
|
LITERATURE CITED |
|---|
 TOP LITERATURE CITED |
|---|
Coyne J. A. W. Meyers A. P. Crittenden P. Sniegowski 1993 The fertility effects of pericentric inversions in Drosophila melanogaster. Genetics 134: 487-496[Abstract]
Darlington C. D. 1939 The evolution of genetic systems. Cambridge University Press, Cambridge, UK
Felber F. J. D. Bever 1997 Effect of triploid fitness on the coexistence of diploids and tetraploids. Biological Journal of the Linnean Society 60: 95-106
Husband B. C. In press The role of triploids in the evolutionary dynamics of mixed-ploidy populations. Biological Journal of the Linnean Society.
Huxley J. S. 1942 Evolution: the modern synthesis. Harper, New York, New York, USA
King M. 1993 Species evolution: the role of chromosome change. Cambridge University Press, Cambridge, UK
Levin D. A. 1975 Minority cytotype exclusion in local plant populations. Taxon 24: 35-43[CrossRef]
Levin D. A. 2000 The origin, expansion, and demise of plant species. Oxford University Press, New York, New York, USA
Mayr E. 1942 Systematics and the origin of species. Columbia University Press, New York, New York, USA
Otto S. P. J. Whitton 2000 Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437[CrossRef][ISI][Medline]
Ozkan H. A. A. Levy M. Feldman 2001 Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-Triticum) group. Plant Cell 13: 1735-1747
Ramsey J. D. W. Schemske 1998 Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 477-501
Rieseberg L. H. 2001 Chromosomal rearrangements and speciation. Trends in Ecology and Evolution 16: 351-358
Soltis P. S. D. E. Soltis 2000 The role of genetic and genomic attributes in the success of polyploids. Proceedings of the National Academy of Sciences USA 97: 7051-7057
Stebbins G. L. 1971 Chromosomal evolution in higher plants. Addison- Wesley, London, UK
Thompson J. D. R. Lumaret 1992 The evolutionary dynamics of polyploid plants: origins, establishment and persistence. Trends in Ecology and Evolution 7: 302-307[CrossRef]
White M. J. D. 1978 Modes of speciation. W.H. Freeman, New York, New York, USA
This article has been cited by other articles:
|
|
 |
|
  F. SELVI, A. COPPI, and M. BIGAZZI Karyotype Variation, Evolution and Phylogeny in Borago (Boraginaceae), with Emphasis on Subgenus Buglossites in the Corso-Sardinian System Ann. Bot., October 1, 2006; 98(4): 857 - 868. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
