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Book Review |
Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California 93106 USA
"... to throw some light on the origin of species—that mystery of mysteries."—Darwin (1859, p. 1)
The path to understanding the mystery of the origin of species has taken a meandering route over the past 150 years. Darwin argued that natural selection worked within species to bring about adaptation and then inferred that this was the early stage of a continuum, eventually leading to speciation. Thus, as the title of his book reflected, he advocated a central role of natural selection in the origin of species. However, during the Modern Synthesis, the founders, such as Mayr, downplayed the role of natural selection in speciation and advocated instead important roles for genetic drift and genetic revolutions, often preceded by founder events. And now, during the last 20 years or so, we have largely returned to Darwin's position that natural selection plays a central role in the origin of species (Schluter, 2000
; Rieseberg et al., 2002
, 2004
).
During these transitions, botanists and studies of plants have had varying degrees of influence. Darwin, of course, was eclectic in both his own studies and the cases he used to illustrate points, as he drew examples from both animal and plant taxa. The main pioneers of the Modern Synthesis (e.g., Mayr, Dobzhansky, Wright, Muller, and Simpson), however, were animal biologists, who, by and large, ignored or minimized the contributions that botany could make to the field of speciation, or how plants may differ from animal systems. This was one of the reasons that led Verne Grant, first in 1971 and then in 1981, to publish his book Plant Speciation (Grant, 2004
). Perhaps with this history, it is not surprising that some botanists waited with at least curiosity, if not trepidation, upon hearing that two fruit-fly geneticists were writing a new book on speciation. How would they treat plants?
Coyne and Orr's Speciation is an exceptionally readable, highly scholarly endeavor reviewing a large amount of research, especially that since about 1980. During this time, research in speciation has burgeoned, and Coyne and Orr provide a clear, systematic, and lucid synthesis of this work, which is quite an accomplishment. In nearly all sections of the book, they first posit the central issues, then outline the theoretical underpinnings, and then provide the relevant evidence, from both laboratory and field studies. They end with conclusions as to what we know now and the future studies that are necessary. In doing so, they elucidate areas that are now generally accepted, such as the role of natural selection in speciation, and illuminate areas that clearly need further investigation. They embrace the past contributions made by botanists and the promise that plant systems hold for unlocking the remaining mysteries of the process of speciation. For instance, they repeatedly utilize plants to exemplify their points and indicate the superiority of plants for studies of processes such as parapatric speciation, habitat isolation, and reinforcement. This does not mean that the authors shied away from making bold and controversial stands, but in doing so they have provided an engaging synthesis of where the field now stands and the directions they feel researchers should undertake in the future.
Speciation begins with a consideration of whether species are, in fact, real and, after deciding that they are, moves on to a spirited defense of the biological species concept (BSC). While Coyne and Orr recognize that no one species concept will satisfy all biologists or situations, they argue that, for sexually reproducing organisms, the BSC has many advantages to understanding the process of speciation (in an appendix they provide a very useful review and critique of other species concepts). Rather than adhering to a strict interpretation of the BSC, they advocate a more relaxed version in which some gene flow can occur between nascent species. While they recognize that this results in subjective interpretations, they argue that it allows for a sliding scale between taxa that are "species-like" and those that are "good species" (i.e., those with no gene flow). Clearly, the use of the BSC has motivated an incredibly productive research program into the nature and evolution of reproductive isolation. What their more relaxed definition does is to focus attention on the area they feel is now central to understanding the process of speciation, i.e., elucidating which isolating barriers have evolved that resulted in the cessation of gene flow. After gene flow has stopped, isolating barriers can continue to evolve but will have had nothing to do with the speciation process itself. Thus, only by studying species that have not yet attained the status of "good species" will we be able to understand the process of speciation.
However, their embracing of the BSC seems to have led Coyne and Orr to several intriguing conclusions, especially about the nature of plant species and the processes that produce them. A particularly startling supposition they make is that the evolution of self-pollination does not constitute the evolution of reproductive isolation and therefore that selfing species do not exist. They argue that self-pollination reduces gene flow among selfers just as much as it reduces gene flow between selfers and their progenitors. Thus, they conclude that the evolution of selfing simply produces "a collection of ‘microspecies,’ with each individual propagating its own genetically isolated lineage" (p. 212).
But what is the evidence for this view? First, it is probably rare for species to be entirely selfing with many lineages evolving independently. Even in Arabidopsis thaliana, there is evidence for floral visitors (Hoffmann et al., 2003
), a low level of outcrossing (i.e., 
1%, Abbott and Gomes, 1989
), and for recombination among alleles, suggesting past sexual reproduction (e.g., Kuittinen and Aguande, 2000
). In fact, in plants, complete selfing occurs extremely rarely, if ever (Vogler and Kalisz, 2001
). This is likely similar in predominantly selfing animal species as well. For example, in C. elegans there is now evidence for occasional outcrossing (Haber et al., 2005
). Even low levels of outcrossing would unite otherwise independent lineages and allow them to evolve together as a species. Individuals of selfing plant species share many traits from flower morphology to habitat associations, suggesting that either there is a highly canalized evolutionary trajectory that each independent lineage must follow or that adaptations within selfing species can spread, via gene flow, allowing the evolution of a good species.
Even if gene flow occurs among individuals of a selfing species, however, Coyne and Orr's argument largely rests on the relative level of gene flow among selfers and between selfers and outcrossers. Recent work in Mimulus suggests that there is asymmetric gene flow from the highly selfing M. nasutus to the outcrossing M. guttatus (Sweigart and Willis, 2003
). The question remains whether this gene flow is greater than that among individuals of M. nasutus and thus whether a selfing mating system has caused reproductive isolation. More studies such as these would be useful.
While Coyne and Orr propose a relaxed view of the BSC, they clearly see the possibility of large-scale hybridization and introgression between sympatric species as a problem. Thus, they generally offer alternative explanations for evidence that indicates a good deal of gene flow among recognized species. For instance, they suggest that hybridization in plants is overestimated because it is due to human disturbance and "the tendency of some botanists to collect along roadsides" (p. 43). In addition, they posit that incongruent phylogenies based on cpDNA or mtDNA may be misleading as to the degree of incongruent nuclear markers. Of course, as yet, few phylogenies are based on multiple nuclear gene genealogies, but two recent studies, one on perennial soybeans (Doyle et al., 2004
) and the other on cotton (Cronn and Wendel, 2004
), suggest that there is evidence of a good deal of hybridization and introgression in the history of these lineages. In 1981 Grant posited a central role of hybridization in plant speciation, and it is now increasingly apparent that different regions of the genomes of plants may experience quite different levels of gene flow. To address the degree of reticulation during speciation, we need both more phylogenetic studies of multiple nuclear genes and studies of how the extent of introgression varies among genomic regions.
One of the core issues that Coyne and Orr recapitulate throughout their book is that we need to understand which isolating barriers actually lead to the cessation of gene flow between species and the order in which they evolve. To do this, we will also need detailed phylogenies at and below the species level. Here the authors suggest that within-species phylogenies will be impossible to reconstruct because gene flow will be too great and will homogenize distinct population histories. However, a recent review on gene-flow estimates suggests that the homogenizing effect of gene flow may vary among gene regions; homogenizing neutral alleles, allowing highly advantageous alleles to rapidly spread, but allowing local adaptation to proceed (Morjan and Rieseberg, 2004
). Thus, depending on the extent of genes involved with local adaptation, examination of multiple gene genealogies may in fact allow us to identify historical patterns below the species level.
Early in their book, Coyne and Orr provide two chapters on the geography of speciation. Not surprisingly, they find a good deal of evidence for allopatric speciation. They conclude, however, that it is difficult to determine the relative frequencies of vicariant vs. peripatric modes. Of particular interest to botanists are their conclusions about parapatric speciation in which they suggest that, while currently lacking, compelling evidence may be found in phylogeographic analyses of restricted edaphic endemic plants and their sister species. Again, detailed phylogenetic analyses will be necessary and point to the need for new nuclear gene regions that are appropriate for study. In their analysis of sympatric speciation, while finding that recent studies now show that it is theoretically quite feasible, they find few examples where it is highly plausible.
Botanists will likely read the chapter on polyploidy and hybrid speciation with special interest. Coyne and Orr give an excellent review of this literature (a similar feat would be for botanists to review the Drosophila literature on postzygotic isolation). While they find that polyploid speciation is largely a phenomenon in plants, rare instances of polyploidy in animals may have played a role in their diversification as well. For instance, recent genome sequencing has revealed a genome duplication event in the early evolution of teleost fish. This has led to speculation of how this duplication may have affected their subsequent diversification into nearly half of all extant vertebrate species (Volff, 2005
).
Coyne and Orr also consider recombinational speciation, or diploid hybrid speciation, and find that while recent theory supports its possibility, its frequency in nature is unclear. Here they downplay evidence that hybrids are not universally unfit as found in surveys of natural plant and animal systems and thus that these hybrids could play a role in generating new species (Arnold and Hodges, 1995
; Arnold, 1997
). They suggest that the vast majority of hybrid crosses yields catastrophic fitness effects and that these surveys focused only on systems where natural hybrid zones form, biasing the data (Day and Schluter, 1995
). However, in order to determine whether hybridization has been important in speciation, it is important to focus on systems where speciation has not gone to completion. In these cases, they conclude that the rare production of fit hybrid genotypes necessary for hybrid speciation is satisfied. Other evidence for past reticulation events comes from multiple gene genealogies as noted earlier and, for example, the detailed analyses and experimental evidence amassed by Rieseberg and colleagues in Helianthus. Their skepticism of the relative importance of this mode of speciation is warranted given the few clear-cut cases from nature, though many more cases need to be investigated.
The last chapter of Speciation delves into broad patterns of speciation, including speciation rates and whether "key characters" promote speciation. It is clear here and throughout their book that Coyne and Orr find comparative studies particularly powerful and enlightening. These types of studies do provide strong evidence for particular patterns and the processes that underlie them by finding significant associations across multiple lineages for increased species diversity in clades that have a particular trait as compared to their sister-taxa that do not. Coyne and Orr are typically cautious in seeking studies that suggest changes in species diversity are due to increased speciation as opposed to decreased extinction. They find two situations convincing, traits increasing sexual selection in animals and traits promoting animal pollination in plants. They conclude that these studies "may allow us to infer which isolating barriers are primary causes of speciation" (p. 441).
However, these comparative studies rely on correlations and therefore will require additional studies and tests to determine if the conclusions from them are accurate. As such, they are but a first step to understanding the process of speciation. As Coyne and Orr themselves point out throughout their book, it is unlikely that a single type of isolation mechanism is responsible for complete reproductive isolation and speciation, and the combined effects of several mechanisms are likely to be needed for speciation to become complete. Thus for example, traits that promote animal pollination may promote increased rates of speciation but may neither be the primary isolating mechanism nor the first mechanism to evolve. Traits promoting animal pollination may simply add another mechanism to a repertoire available to achieve speciation and in doing so increase the frequency of speciation and the speed at which it is attained. To answer these questions, we need detailed species phylogenies to test the frequency that speciation is associated with shifts in particular traits, such as animal pollination of plants as compared to other forms of reproductive isolation. In addition, more studies on the strength of each type of reproductive isolation between species (e.g., Ramsey et al., 2003
) will be essential to determine their relative importance.
While Speciation is filled with suggestions of future research and makes clear many issues that have been substantially resolved and those that have not, it is reasonable to ask what are the areas where studies of plants can be particularly useful? Unbiased as I may try to be, the question may more easily be asked as to whether there are any areas where they will not continue to be at the forefront. Because of their largely sedentary nature, plants are ideal for addressing the issues of how habitat isolation has played a role in speciation. Given that ecotypic differentiation within species is usually associated with habitats (Clausen et al., 1940
) and that many sister taxa also differ in their habitats, habitat isolation is likely to be a major component of speciation. Transplant studies are critical to test the degree of habitat isolation, and obviously, this is much easier in plant as compared to animal systems. These studies need to be done in a variety of systems and between taxa at different degrees along the continuum to speciation. A particular advantage of such studies is that, though they are not necessarily easy experiments, they require little high-tech equipment and are therefore possible to conduct by most researchers. Similarly, isolating mechanisms that occur post-pollination and pre-fertilization are ripe for future studies as they have been studied in relatively few taxa and their general importance to speciation is unclear. More studies are also needed on the role that hybridization plays in producing novel phenotypes and how both intrinsic and extrinsic selection acts on hybrid individuals. Because initial polyploids can be synthesized, particularly interesting studies will be possible on how reproductive isolation between ploidy levels (e.g., Husband and Sabara, 2003
) evolves.
At the genomic level, plants will also provide excellent systems to elucidate the genetic basis of reproductive isolation. Coyne and Orr cite four studies where the actual genes involved in postzygotic isolation have been identified, three in Drosophila and one in a species of fish. These isolation genes show the hallmarks of positive selection and reinforce the view that speciation is driven by natural selection. Another tentative conclusion is that not all of these genes are regulatory in nature. However, as they point out, the sample size is rather small. To answer questions about the molecular basis of speciation, we will need data on the genes underlying all types of reproductive isolation and from many different taxa. Given the advantages of plants for determining which types of isolation are important during the process of speciation, they will also serve especially well for determining the genetic basis of various forms of reproductive isolation.
Several plant systems have already been or are being developed (e.g., Helianthus, Mimulus, and Aquilegia) to provide the necessary infrastructure to identify the genes underlying traits causing reproductive isolation. These resources include detailed genetic maps, physical maps, and EST sequencing. As each of these groups is fairly species-rich, they will provide the resources for investigating many instances of speciation and the opportunities for a large number of studies. These groups are, of course, in addition to model systems such as Arabidopsis and many crop species for which genomic resources are already developed. Extending these resources to their wild relatives will only enhance our ability to understand the process of speciation. Given the extremely rapid pace of technology development, we can look forward to greater ease and lower costs of dissecting the genetic basis of traits in other non-model organisms as well. Thus, in the next 10 to 20 years, we will likely begin to amass the evidence necessary to answer questions such as whether the genes involved with initiating and enhancing reproductive isolation are regulatory or structural, whether the mutational differences underlying them are in coding or noncoding regions, whether transposable elements play a role in speciation, and whether specific types of genes are more likely to be involved with different forms of reproductive isolation.
Speciation richly documents that the field has recently made tremendous progress, and Coyne and Orr's synthesis is especially timely. They clearly expect a high level of scholarship from those who read their book; they do not always spend time explaining specific concepts or definitions. It will be an excellent book for graduate seminars, where it will likely spark debate and inspire the future leaders of the field. In fact, it will undoubtedly become the new bible for the field. This poses a challenge for readers to examine the data as carefully as Coyne and Orr have done and then to confront the conclusions they have drawn, because this will surely move us forward in our understanding of the origin of species.
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FOOTNOTES |
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2 E-mail: hodges{at}lifesci.ucsb.edu
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LITERATURE CITED |
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 TOP LITERATURE CITED |
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Arnold M. L. 1997 Natural hybridization and evolution. Oxford University Press, New York, New York, USA
Arnold M. L. S. A. Hodges 1995 Are natural hybrids fit or unfit relative to their parents?. Trends in Ecology and Evolution 10: 67-71
Clausen J. D. D. Keck W. M. Hiesey 1940 Experimental studies on the nature of species. I. Effect of varied environments on western North America plants. Publication 520, Carnegie Institute of Washington, Washington, D.C., USA
Cronn R. J. F. Wendel 2004 Cryptic trysts, genomic mergers, and plant speciation. New Phytologist 161: 133-142[CrossRef][ISI]
Darwin C. R. 1859 The origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. J. Murray, London, UK
Day T. D. Schluter 1995 The fitness of hybrids. Trends in Ecology and Evolution 10: 288
Doyle J. J. J. L. Doyle J. T. Rauscher A. H. D. Brown 2004 Diploid and polyploid reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine). New Phytologist 161: 121-132[CrossRef][ISI]
Grant V. 1981 Plant speciation, 2nd ed. Columbia University Press, New York, New York, USA
Grant V. 2004 Plant speciation, the book: perspectives and paradigms. New Phytologist 161: 8-11[CrossRef][ISI]
Haber M. M. Schüngel A. Putz S. Müller B. Hasert H. Schulenburg 2005 Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Molecular Biology and Evolution 22: 160-173
Hoffmann M. H. M. Bremer K. Schneider F. Burger E. Stolle G. Moritz 2003 Flower visitors in a natural population of Arabidopsis thaliana. Plant Biology 5: 491-494[CrossRef][ISI]
Husband B. C. H. A. Sabara 2003 Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytologist 161: 703-713[CrossRef][ISI]
Kuittinen H. M. Aguade 2000 Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana. Genetics 155: 863-872
Morjan C. L. L. H. Rieseberg 2004 How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles. Molecular Ecology 13: 1341-1356[CrossRef][Medline]
Ramsey J. H. D. Bradshaw D. W. Schemske 2003 Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Scrophulariaceae). Evolution 57: 1520-1534[CrossRef][ISI][Medline]
Rieseberg L. H. A. Widmer A. M. Arntz J. M. Burke 2002 Directional selection is the primary cause of phenotypic diversification. Proceedings of the National Academy of Sciences, USA 99: 12242-12245
Rieseberg L. H. S. A. Church C. L. Morjan 2004 Integration of populations and differentiation of species. New Phytologist 161: 59-69[CrossRef][ISI]
Schluter D. 2000 The ecology of adaptive radiation. Oxford University Press, Oxford, UK
Sweigart A. L. J. H. Willis 2003 Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression. Evolution 57: 2490-2506[CrossRef][ISI][Medline]
Vogler D. W. S. Kalisz 2001 Sex among the flowers: the distribution of plant mating systems. Evolution 55: 202-204[CrossRef][ISI][Medline]
Volff J. N. 2005 Genome evolution and biodiversity in teleost fish. Heredity 94: 280-294[CrossRef][ISI][Medline]
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