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, 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 of the process by which polyploids and spread in populations of their and While Levin to summarize research in these he never the current nor does he them to of polyploid speciation. Chapter 6 is devoted to the evolutionary dynamics of polyploidy. It begins with a review of the of polyploid evolution. As Levin the of gametes is the mechanism of polyploid the evidence for this is gametes and are by plants and variation in formation has a large genetic and environmental However, most of our knowledge from plants, whereas the magnitude and role of gametes in natural populations is Moreover, the between the frequency of gametes and the number of polyploid in the in the of a potential mechanism 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 explanation 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 suggest that in a surprising 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 gametes in natural populations and for rates of In addition, highly variable markers such as will be to the origins 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 contributions to this Levin the by the theoretical barriers to establishment as a result of the low fitness of and a frequency-dependent mating This has numerous empirical and further theoretical studies of ecological and genetic factors that may overcome this barrier, including ecological and However, research on these topics is to a few model systems and little has been to or directly to polyploid establishment in natural populations. of mating this very studies of flowering between have reproductive isolation, and a few studies on suggest the However, there are no studies of the reproductive barriers between and that the relative importance of mechanisms or their effects on polyploid Moreover, Levin that mating will however, recent including one of his suggest this is not the In other more is to understand both the theoretical of these processes as well as their relative contributions in natural populations. In to the factors mentioned that may Levin an ecological specifically that polyploidy can become through the of new rather than in populations. with ecological differentiation this process may be one of the most important and most factors polyploid speciation. the of Chapter Levin describes the of and polyploids. a of he that differences in distribution exist between While I not I a more critical would have that geographic does not necessarily ecological differentiation 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 Similarly, in the discussion of between and Levin does not the distinction between and independent mechanisms for maintaining hybrid This the confusion in the polyploidy literature regarding the of ecological differentiation historical in Unfortunately, most molecular approaches on polyploid 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 question 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 multiplication can However, to we the to these shifts and to understand their underlying genetic To we studies that polyploids to the of their In addition, into polyploids in number may to the effects of gene from the effects of polyploidy. of the problem to is that most studies of species of and These studies are by the that it is to the effects of chromosome from the effects of selection to the polyploids will be essential for this but have not been enough in this chapter. markers have our understanding of plant evolution through polyploidy in many As Levin and DNA have provided valuable tools for polyploid 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 multiple origins of many polyploid both and origins provide an explanation for the within polyploid by Levin in Chapter This also that polyploid evolution is more than and is to population which are in Chapter However, that many of these evolutionary studies are not on among Moreover, it is obvious that and polyploids can and do albeit after I with Levin that the will be on researchers to of phylogenetic and geographic data to more between single and and primary and to identify origins of polyploids from populations. In describing the changes in genome and that occur after formation of Levin one of the most exciting in polyploid research the As Levin the that that independent However, research using in hybridization genetic and studies show that extensive rearrangements, gene and translocations can many within the first few their synthesis and et al., et al., The of polyploids for these processes has polyploid 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 valuable 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 whole in more than one Despite I found the relatively to with the of some critical (e.g., genome size, and cytogenetic which more complete As mentioned entire of some chapters out of the difficult 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 might have more to between the various and would have the more and on future One this book for was how research on polyploid and chromosomal evolution have as two It is surprising to how many common theoretical issues (e.g., hybrid 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 valuable For example, having chapters on chromosomal variants is but it the on phenomena rather than on evolutionary processes to which they such as reproductive isolation, evolutionary dynamics, 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 benefited from a introductory chapter that the of the karyotype and the historical role of chromosomal mechanisms of speciation. In addition, a synthesis at or near 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 any the role of chromosomal mechanisms in plant speciation.

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