Chromosomal variation in plant evolution

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, and are for understanding the of rearrangements on fitness and the that rare chromosomal variants will to is not the only by which different chromosomal species may be In fact, fertility can be or even for some chromosomal variants (e.g., for differences in and for mechanisms of 1993; Rieseberg, 2001). In these cases, hybrids can of that may impact the dynamics of chromosomal variants in and hence the of fixing a novel is less than has that the most important impact of chromosomal rearrangements on may be through their on models that gene flow will in to the fitness recombination rates are to be lower in of chromosomes. empirical studies of between two species of this and that rearrangements of large may gene flow extensive chromosomal The of chromosomal rearrangements on are central to discussion on speciation. But this issue does not the many of this issue and the of whether chromosomal variants are the basis for species Unfortunately, this controversy is never dealt with in this or other chapter. As the major to a role for chromosomal speciation is that it is for a novel to be fixed in populations. However, and at the of there are a number of models that have factors that overcome this such as meiotic accumulation of rearrangements, and ecological among chromosomal variants in King, 1993; Rieseberg, 2001). the significance of or the of associated with chromosomal variation has not been but may speciation by the impact of rare cytotypes and strong In this book, no attention is to these or to general for or chromosomal speciation. This is given Levin's many to our understanding of population plant evolution. book on chromosomal evolution in plants would be without mention of permanent translocation heterozygosity, and Levin devotes the chapter to this Here, he describes its evolutionary genetic and provides a brief discussion of how such may in the For the he describes two major one accumulation of translocations in and the between races or than species in the number of translocations they the evidence for the that early translocations result in reduced fertility in it is how they would long to an accumulation of In the more of the population and the significance of would be useful for a description of these hypotheses. Most it is clear that the full force of contemporary molecular have not been to on this topic and therefore this section would have from a more general discussion of the for future Chapters 6 through various aspects of the of chromosome estimates this represents one of the single most common evolutionary changes in the genetic system of plants not and many prominent refer to it as one of few mechanisms of speciation other chromosomal variants, however, the is out with to its contribution to species As Levin points our current estimates of polyploidy are likely as and genetic that taxa are often and that many species, viewed as are likely In the of in a phylogenetic context may that the number of of polyploids is Despite its prevalence, there are no estimates of the of speciation associated with polyploidy and 2000) and no of the by which polyploids and in of their and While Levin to summarize research in these he never the current nor does he them to of speciation. Chapter 6 is devoted to the evolutionary dynamics of polyploidy. It begins with a review of the of evolution. As Levin the of is the of the evidence for this is and are by plants and variation in formation has a large genetic and environmental However, most of our knowledge from plants, whereas the and role of in natural is the between the frequency of and the number of in the in the of a potential with its relative importance in the the in Levin evaluates the role of through the by the causes for of I have to a clear for the in a book or and this was no by on causes of Levin the that are often and and and can play an important role as in formation recent studies that in a number of polyploidy taxa and that their contribution can be even when their are low and in However, with relatively little empirical research in this our knowledge of the rates and of polyploidy formation in the cytometry will provide some by a of and in natural and for rates of In addition, highly markers such as will be to the of and to from the To this has not been to research on chromosomal rearrangements, researchers have some into the evolutionary forces the establishment of in due to Levin's to this Levin the by the theoretical barriers to establishment as a result of the low fitness of and a frequency-dependent This has numerous empirical and further theoretical studies of ecological and genetic factors that may overcome this including ecological and However, research on these topics is to a few model systems and little has been to or directly to establishment in natural populations. of this very studies of flowering between have and a few studies on the However, there are no studies of the barriers between and that the relative importance of mechanisms or their on Levin that will however, recent including one of his this is not the In other more is to understand both the theoretical of these as well as their relative in natural populations. In to the factors that may Levin an ecological that polyploidy can become through the of new rather than in populations. with ecological this may be one of the most important and most factors speciation. the of Chapter Levin describes the of and a of he that differences in distribution exist between While I not I a more critical would have that does not necessarily ecological and that many of the from this data have been on studies that do not for Therefore, the data provides a of about the association between polyploidy and either breadth of ecological or to or in the discussion of between and Levin does not the distinction between and mechanisms for This the confusion in the polyploidy literature regarding the of ecological historical in Unfortunately, most molecular approaches on systems have not a strong which is to identify primary and more there is not a single published in which and polyploids have been as a of between adaptive and historical In Chapter Levin describes the many and ecological differences between polyploids and This is important for understanding the adaptive significance of polyploidy. In general, the chapter is a of a of but there is no obvious to synthesize or evaluate this we to understand whether chromosome can However, to we the to these shifts and to understand their genetic To we studies that polyploids to the of their In addition, into polyploids in number may to the of gene from the of polyploidy. of the problem to is that most studies of species of and These studies are by the that it is to the of chromosome from the of to the polyploids will be for this but have not been in this chapter. markers have our understanding of plant evolution through polyploidy in many As Levin and DNA have provided for variation and for between from within a single species and from hybridization between species have been as relatively rare perhaps because of the between and their and due to the and cytogenetic on which their are the of as a result of molecular studies that the of may be as much a problem as result from approaches has been the evidence for the of many both and provide an for the within by Levin in Chapter This also that evolution is more than and is to population which are in Chapter However, that many of these evolutionary studies are not on among it is obvious that and polyploids can and do albeit after I with Levin that the will be on researchers to of phylogenetic and data to more between single and and primary and to identify of polyploids from populations. In describing the changes in genome and that occur after formation of Levin one of the most exciting in research the As Levin the that that However, research using in hybridization genetic and studies that extensive rearrangements, gene and translocations can many within the few their synthesis and The of polyploids for these has research to the of evolution and is our of polyploids as evolutionary The exciting insights that are being however, only the of this new polyploids will also provide a on the rapid evolutionary of that are of significance to and speciation. In this book is a of information on many different aspects of chromosomal variation in plants. It is heavily and is well having on the The book was well although there a number of and in more than one Despite I found the relatively to with the of some critical (e.g., genome size, and cytogenetic which more As entire of some chapters out of the to follow at The large number of examples the book would be an however, I would have given some in place of more both within topics and in the context of speciation. more time devoted to future research have more to between the various and would have the more and on future One this book for was how research on and chromosomal evolution have as two It is to how many common theoretical issues (e.g., at the of these two especially as they to speciation, and how they have being the of this book was not to such integration and a For example, having chapters on chromosomal variants is but it the on phenomena rather than on evolutionary to which they such as evolutionary and speciation. To be Levin to between the evolutionary dynamics of polyploids and chromosomal it was very brief and within a section in Chapter At the very the book would have from a introductory chapter that the of the karyotype and the historical role of chromosomal mechanisms of speciation. In addition, a synthesis at or the would have provided a to the major evolutionary and to among the different kinds of chromosomal The lack of integration among theoretical and empirical research on different kinds of rearrangements how much we can understand with the role of chromosomal mechanisms in plant speciation.

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