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Book Review |
Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794-5245 USA
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INTRODUCTION |
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 TOP INTRODUCTION MICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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One way to make sense of the diversity embodied in the book is to group the chapters into either a macroevolutionary or microevolutionary (population genetic) emphasis. Most studies emanating from "evo-devo" tend to examine phylogenetic patterns of evolution to understand homology of structure and developmental processes, clearly a "macroevo-devo" approach (to coin a phrase). This book is no exception; all but two of the data chapters deal primarily with macroevolutionary patterns. On the other hand, population geneticists increasingly are realizing that developmental biology is essential to generate a theory of variation (Stern, 2000
) or to deal with epistatic interactions in phenotypic evolution (Rice, 2002
). The contributions of Gillies et al. (chapter 12) and McLellan et al. (chapter 16) adopt a microevo-devo perspective to the study of phenotypic variation.
Another way to group the chapters is whether they are primarily designed to answer developmental or evolutionary questions. Most of the contributions focus on evolution, but two discuss the use of phylogenies to understand developmental process (chapter 3, by Hawkins, and chapter 15, by Doust and Kellogg). In this book, the idea that evo-devo studies could be used to determine the relative explanatory power of developmental genetic and population genetic forces in evolution is not examined (Wagner, 2000)
.
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MICROEVOLUTION AND MACROEVOLUTION |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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Phyletic
The phyletic criterion is unambiguous: patterns and processes at the population level are microevolutionary; those at species level and above are macroevolutionary. This criterion can be used to establish whether or not there are patterns of variation across species that cannot be recognized from variation within species. The patterns are best characterized in a phylogenetic context so as to be considered unambiguous macroevolutionary patterns.
Whether phenotypic variation is perceived as "micro" or "macro" may differ depending on whether the study has a developmental genetic, morphological, or evolutionary point of view. For instance, variation in conical cells of petals (Antirrhinum: chapter 8, by Glover and Martin) may be "micro" in morphological terms, but may be correlated with speciation, thus having macroevolutionary implications; on the other hand, "macro" morphological differences between leaves (Begonia: chapter 15, by Doust and Kellogg) may not show such correlations. Microevo-devo studies use population polymorphisms, a pattern of variation that does not need interspecific comparisons; macroevo-devo studies use homology and homoplasy, which cannot be established without interspecific comparisons in a phylogenetic framework.
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THE GENETIC BASIS OF PHENOTYPIC VARIATION |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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McLellan et al. (chapter 16) present two points regarding the genetics of development: (1) A perusal of eight QTL studies indicates that most morphological structures are under the control of 18–74 genes. This number is larger than the single gene of major effects touted by several botanists (e.g., Bateman and DiMichele, chapter 7), but much smaller than the infinite genes models of population geneticists and, therefore, is characterized as "oligogenic" by the authors. (2) The development of morphological structures is controlled by a few primary genes, which "result in alterations to developmental pathways and their morphological results," and by downstream target genes of primary genes, secondary genes, whose expression is modified because of an inherited change in primary genes. Primary genes are the drivers of evolutionary change in morphology. This framework and terminology has been adopted by several of the contributors. McLellan et al. point out, that given the number of QTLs may be as many as 74, the candidate gene approach might not work in all cases. Baum (chapter 25) makes a clear and useful presentation of experimental approaches under the candidate gene approach. He discusses sampling strategies, alternative results that might be expected in each case, and possible interpretations of the results. These two chapters will be useful for evolutionarily naïve and not-so-naïve researchers and make good reading for beginning students as well.
Cox (chapter 24) presents the fascinating developmental variation in the sculpting of diatom walls and makes a case for using diatoms as a model system for studying developmental traits at the cellular level. This chapter also serves to draw attention to obvious limitations in the phylogenetic range of model organisms studied; there is little indication of much activity even in favorite experimental systems of yore, e.g., Fucus and Chlamydomonas; Acetabularia may be an exception (Serikawa and Mandoli, 1999
).
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THE DEVELOPMENTAL GENETICS OF PHENOTYPIC VARIATION |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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Examining these conceptual terms within a broader framework reveals their relationships with one another (Table 1). Interspecific patterns (column 4) in the upper part of the table conceivably can be related to patterns or processes listed as intraspecific. The interspecific patterns of homology and homoplasy cannot be studied within populations. They clearly are based on genetic developmental pathways and networks. The question, "What are the factors that serve to either change or maintain these networks?," is at the heart of the evo-devo effort. "Novelty" receives only passing mention in a few chapters, perhaps because it is a general umbrella term for concepts like heterotopy. Chapters 6–13, mostly on floral development, and chapters 17–23 on vegetative development are conveniently examined using this framework. Chapters 3, 15, and 16 illustrate the potential gains of thoughtful morphological analyses and are discussed separately.
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). Perhaps the small number of examples for the latter two types of change is simply because they are more difficult to demonstrate experimentally than is paralogy. The genetic basis of polymorphism in leaf form is demonstrated using AFLP methods to identify QTL markers in Begonia dregei (chapter 16, by McLellan et al.). Floral symmetry in Layia and Senecio, previously known from morphological genetic analysis to be controlled by one or two genes, is being investigated using CYCLOIDEA as the target gene (Gillies et al.). These two chapters alone present data on intraspecific variation that potentially are informative in the understanding of microevolution.
In all other chapters, evolutionary inferences are based on the study of interspecific variation and comparisons across species and therefore are taken to represent studies in macroevolution even though similar inferences could, in theory, be made through the study of intraspecific variation (representing microevolutionary study). Glover and Martin (chapter 8) investigate conical cells on the surface of petals, which influence pollinator attraction and are variably present across taxa, including families. The authors show for the MYB gene Mixta, which controls this trait, that paralogous genes in Antirrhinum act at different times in development and have different effects; in transgenic experiments, high levels of overexpression in Nicotiana cause trichome development and lower levels promote conical cells. The gene does not have the same effect in transgenic Arabidopsis. This last example suggests that different processes prevail in asterids and rosids. Cubas (chapter 13) discusses the TCP gene family, which includes TB1 (source of the "Doebly hypothesis" regarding the evolutionary role of cis-regulatory elements) and CYCLOIDEA, which controls dorsiventral symmetry in flowers of several Lamiales (e.g., Antirrhinum, Gesneriaceae). Knapp (chapter 14) points out that Solanaceae follow "Robyns' rule" (the abaxial stamen is lost first, in contrast to what is seen in Lamiales). The inflorescence branches by bifurcation in Solanum and Petunia, but not in Antirrhinum. Because the type of inflorescence and type of floral symmetry may be developmentally correlated (Coen and Nugent, 1994
), Knapp makes the testable prediction that, if CYC is involved in determining the type of floral symmetry, it should operate differently in Solanaceae when compared to the Lamiales. All three chapters show that paralogues of different genes may evolve at different rates and that expression may diverge beyond comparison in some cases, as has been discussed for other genes (Haag and True, 2001
).
And now the ABC, make that ((A, E),(B, Bsis)),(C, D), of floral development: The critical importance of gene duplication in the diversification of function is clearly demonstrated in chapters 9–11. Theissen et al. (chapter 9) present an engrossing, if packed, summary of the state of the art, aided by the clarity of distinguishing between "A-genes" and "A-function." From a mere one or two copies, the MIKC-MADS box genes had multiplied to at least six paralogues in the seed plant ancestor, so: (((A/E),(B, Bsis)),C/D). In "gymnosperms," A/E expression is general (Johansen et al., 2002), C/D expression distinguishes reproductive from vegetative shoots, male shoots are (B+ Bsis–) and female shoots are (B– Bsis+). In angiosperms, to grossly simplify a complex story, C and D genes are co-opted for carpel and ovule functions, and E genes seem to be "liberated" to take on other functions. Thus, Johansen and Frederiksen (chapter 10) show, using expression patterns, that in orchids E genes are expressed in the viscidium and tegula, suggesting a role in the diversification of these specialized extensions of the stigma. Teeri et al. (chapter 11) convincingly demonstrate, using transgenic Gerbera, that E genes have a C function in these flowers.
What of flowers themselves? Frohlich (chapter 6) and Theissen et al. (chapter 9) agree that the "anthophyte" hypothesis is out and that flowers probably evolved from unisexual reproductive shoots. Frohlich provides arguments, using the orthology-paralogy relationships of LFY genes, which have two copies in "gymnosperms" but only one in angiosperms, to support the hypothesis that bisexual shoots arose from the male shoot. Theissen et al., on the other hand, use the ABCDE model to argue for an origin from female shoots. Both pose hypotheses that are testable, and results that enable this testing are likely to come soon. The "abominable mystery" is in the process of being deconstructed.
The vegetative form of plants has attracted far less evo-devo attention (three chapters) than floral development (10 chapters), but this situation is changing, as may be seen by the fact that two chapters (19, 20) discuss newly initiated studies on nonflowering plants. While floral evolutionary studies are not handicapped by the angiosperm-centric field of developmental genetics, evolutionary understanding of vegetative structure is. Schneider et al. (chapter 17) use a phylogenetic definition of body plans as synapomorphies to then identify different types of body plans in vascular plants. Their results may be difficult to interpret in practice—for instance, in identifying the developmental processes that operate in a body plan whose variable components are meristem structure, sporangium position, sporangium wall development, and life cycle.
Tsiantis et al. (chapter 22) discuss leaf development in angiosperms. The knox genes are homeobox genes with a critical role in maintenance of the shoot apical meristem (SAM) and an additional one in leaf development. In the latter role, knox genes may be involved in two different pathways: one that determines leaf identity and the other, elaboration of the lamina. Components of the knox pathway are just beginning to be understood; they include upstream regulation by a group of MYB genes, AS1/rs2/PHAN (ARP in chapter 19, by Langdale et al.) and downstream genes that regulate gibberellins that, in turn, affect later leaf development. Evolution of leaves is examined through a morphological lens by Rudall and Buzgo (chapter 23) and Gleissberg (chapter 21). Rudall and Buzgo describe the complexities of monocot leaves. They emphasize the importance of recognizing a transition zone between the classical upper and lower leaf zones and suggest that adaxial growth in this region in some leaves corresponds to lateral growth of the primordium in maize; if so, this could be tested by using transgenic constructs containing molecular markers. Continuing with the foliar theme, Gleissberg (chapter 21) discusses the role of KNOX in dissected leaf development and of a possible role for PHAN genes in the differentiation of petiolate and nonpetiolate leaves, such as in Papaveraceae.
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DEVELOPMENTAL MORPHOLOGY AND PHENOTYPIC VARIATION |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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), but it is at the primary stage that developmental information is critically needed to improve subsequent phyologenetic analysis (whether mapping the characters onto trees or using them to build trees). It is this approach that Doust and Kellogg (chapter 15) bring to their analysis of inflorescence morphology. They characterize morphology in terms of putative or demonstrably process-based developmental components so as to enable developmental-evolutionary interpretation of the phylogenetic results (e.g., Bharathan, 1996
). This process-based characterization is one way to ensure both realistic evolutionary interpretation of development and realistic developmental interpretation of evolution. Doust and Kellogg use this analysis to implement what looks to be a fruitful application of QTL methods to detect the genetic basis of morphological differences between species. To connect with the other QTL study in this volume, that of McLellan et al. (chapter 16), it is worth noting that this work takes off from McLellan's previous morphometric studies of leaf development, which allowed her to detect the general developmental patterns in leaves (McLellan, 1990
). We need more, diverse, careful descriptions of morphology that would allow us to see the changes during evolution.
Hawkins then discusses secondary hypotheses of homology and points out the insights that homoplasy can provide for our understanding of how complex morphologies can re-evolve multiple times (e.g., Kellogg, chapter 2; Bharathan et al., 2002
; Whiting et al., 2003
). It cannot be emphasized enough that macroevolutionary patterns are equally informative as sampling in regard to developmental processes. The angiosperm leaf study, for instance, started with two model species as data points: tomato, which showed involvement of knox in complexity of leaf form, and pea, which did not, with little indication of which pattern, if any, was the more general one. The demonstration that knox was expressed in complex primordia of taxa across angiosperms, with the exception of the pea clade nested within legumes (N. R. Sinha et al., unpublished data), helps to establish a level of generality to the underlying mechanism that might not otherwise be done easily.
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TELOMES, LEAVES, AND THE IMPORTANCE OF "PLACE" |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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Harrison et al. (chapter 20) review the developmental genetic data on angiosperm leaves, concluding that there is little "evidence of distinct genetic control of leafy characters that might reflect stepwise transitions from a branching system." They base this conclusion on the fact that mutations of supposed leaf-specific genes have effects on the shoot as well. For instance, loss of the PHAN gene, thought to be leaf-specific, results in reduced leaf growth, dorsiventral asymmetry, and SAM activity. Similarly, the HD-ZIP III genes have no leaf-specificity. It is not clear why pleiotropic effects preclude the gradual (stepwise) assembly of the network that today generates leaves. One recent piece of evidence does suggest a difference in the way megaphylls were put together in the two lineages. In the seed plant lineage, the site of leaf initiation (Po) is marked by downregulation of Knox, but this is not the case in the ferns studied so far (Bharathan et al., 2002
).
These discussions once again reveal the importance of "place" in the diversification of plant bodies and creating novel structures. The importance of heterotopy (a general term that includes the more common and restrictive ectopy and homeosis) is emphasized in several chapters. It is useful also to note that in diversification of structures, just as genes, a first step often involves duplication (serial homology), resulting in the creation of a new "place" for gene expression ("neotopy," perhaps, to add to the proliferating terminology). Genes normally expressed in the unduplicated structure may or may not undergo change in one of the duplicated structures (loss of function, overexpression, change in timing, etc.). If there were no modification in the duplicated part, then it could survive because of selective value (even though not a morphological novelty, e.g., stamen multiplication), or because the duplication itself is a novelty. One could think of the origin of branching in the original telome to form the branched mesome (Fig. 18.1) as one such event, which enabled elaboration of the plant body and consequent invention of stems, leaves, and roots.
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ENDNOTE |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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came up with a most satisfying explanation to the question of why variation might appear to be greater at times of speciation than at other times. He proposed that because of habitat shifts in time, differentiation among populations was likely to be subsumed by gene flow, whereas reproductive isolation allows morphological variants to be "captured" and further modified within species lineages. "Long-term anagenetic change in some characters is then the consequence of a succession of speciation events" (Futuyma, 1987
). "Futuyma's ratchet" (M. A. Bell and M. Travos, Stony Brook University, unpublished manuscript) shows how differences can accumulate along a lineage. It could explain, for instance, Kellogg's observation that heterochrony, which is more prevalent toward the tips of a phylogeny, may look like heterotopy in the deeper nodes.
The book has clear figures and line drawings and several colorful plates of all manner of morphological variation. The chapters are widely different, e.g., lengths ranging from 13 to 34 pages. There are two useful indices of subject terms and taxon names. The provision of a glossary is an excellent idea to help bridge disciplinary gaps. Some terms crop up repeatedly that could be in the index: body plan, ectopy, gene expression, genetic network, homology, homeosis, homeostasis, novelty, saltation. To the "venting" on asymmetry of flowers and dorsoventrality of structures (p. 128), one could add "phenocopy." A phenocopy is not a mutant or a transgenic that looks like another mutant or transgenic, but is a "phenotype, developed in response to an environmental stimulus, that resembles one known to be produced by a gene mutation" (Futuyma, 1986
).
A book of this sort should help to keep the dialogue going between developmentalists and evolutionists. However, given that the empirical work is almost sure to be dated by the time of publication, it might not attract the attention of the die-hard molecular developmentalists. I hope that is not true, for I think all players in this game can learn from the diverse and interesting perspectives and approaches presented. Would the book be of interest to those who study animal evo-devo? Yes, especially the chapters on QTLs involving interspecific crosses, which are likely to be among the major sources of data in the future on this topic. The intriguing hints of differences in evolution in plants and animals because of differences in genetics (e.g., plants have greater tolerance of transposons and many more QTL genes controlling developmental differences) and arguments that "open" plant systems are more likely to be subject to heterotopy are testable hypotheses for which data are likely to emerge over the next few years. To both groups, I say: it would be worth your while to look at this book.
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FOOTNOTES |
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2 E-mail: geeta{at}life.bio.sunysb.edu
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LITERATURE CITED |
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TOPINTRODUCTIONMICROEVOLUTION AND...THE GENETIC BASIS OF...THE DEVELOPMENTAL GENETICS OF...DEVELOPMENTAL MORPHOLOGY AND...TELOMES, LEAVES, AND THE...ENDNOTELITERATURE CITED |
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Bharathan G. T. Goliber C. Moore S. Kessler T. Pham N. Sinha 2002 Homologies in leaf development inferred from KNOXI gene expression. Science 296: 1858-1860
Coen E. S. J. S. Nugent 1994 Evolution of flowers and inflorescences. Development (Supplement) 1994 107-116
Futuyma D. J. 1986 Evolutionary biology, 2nd ed. Sinauer, Sunderland, Massachusetts, USA
Futuyma D. J. 1987 On the role of species in anagenesis. American Naturalist 130: 465-473[CrossRef][ISI]
Golz J. F. E. J. Keck A. Hudson 2002 Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum. Current Biology 12: 515-522[CrossRef][ISI][Medline]
Haag E. S. J. R. True 2001 From mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biology. Evolution 55: 1077-1084[CrossRef][ISI][Medline]
McLellan T. 1990 Development of differences in leaf shape in Begonia dregei (Begoniaceae). American Journal of Botany 77: 796-801
Patterson C. 1988 Homology in classical and molecular biology. Molecular Biology and Evolution 5: 603-625[Abstract]
Rice S. H. 2002 A general population genetic theory for the evolution of developmental interactions. Proceedings of the National Academy of Sciences (USA) 99: 15518-15523
Serikawa K. A. D. F. Mandoli 1999 Aaknox1, a kn1-like homeobox gene in Acetabularia acetabulum, undergoes developmentally regulated subcellular localization. Plant Molecular Biology 41: 785-793[CrossRef][ISI][Medline]
Stern D. L. 2000 Evolutionary developmental biology and the problem of variation. Evolution 54: 1079-1091[CrossRef][ISI][Medline]
Wagner G. P. 2000 What is the promise of developmental evolution? Part I. Why is developmental biology necessary to explain evolutionary innovations?. Journal of Experimental Zoology (Mol Dev Evol) 288: 95-98
Whiting M. F. S. Bradler T. Maxwell 2003 Loss and recovery of wings in stick insects. Nature 421: 264-267[CrossRef][Medline]
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