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Book Review |
Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4
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INTRODUCTION |
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 TOP INTRODUCTION LITERATURE CITED |
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There is a grandeur to this view of life ... that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved.—Darwin, 1859, p. 490
In this closing sentence from The Origin of Species, Darwin identified the most fundamental problem in biology and his solution to that problem. The problem is to explain the diversity of life, both the number of species and their phenotypic variety. Darwin's explanation was evolution, by which he specifically meant natural selection. Nevertheless, much of The Origin of Species considered change within species, rather than speciation or the diversification of species. In large measure, this focus reflected Darwin's expectation that speciation accompanies differential adaptation to local environments in different areas of a species' range. Thus, the process of speciation does not differ fundamentally from that responsible for adaptive geographic variation within species.
As conceived by Darwin, natural selection results when three conditions occur together: phenotypic variation, differences in performance (fitness) between dissimilar phenotypes, and heritable resemblance of offspring to their parents. As a result of these conditions, average performance in a population increases with time, because the heritable characteristics of individuals that fail to survive or leave few offspring are not represented in subsequent generations. This adaptation to the prevailing environment therefore results from a combination of ecological interaction, which determines performance, and genetics. Darwin successfully characterized adaptation by natural selection, despite his erroneous conception of genetics, because genetic details, other than heredity itself, influence general outcomes much less than ecology. Consequently, Darwin could apply his prodigious ability as an experimental natural historian to interpret a bewildering array of adaptations in the many books that he published after The Origin of Species.
As its title indicates, Dolph Schluter's book, The Ecology of Adaptive Radiation, continues the Darwinian approach of seeking the explanation of species diversity in the association between phenotype and ecological performance. In particular, Schluter evaluates the "Ecological Theory" of adaptive radiation elaborated roughly a century after The Origin of Species, largely through the work of Dobzhansky, Lack, and Simpson. This theory depicts adaptive radiation as the combined outcome of three processes, all of which foster phenotypic diversification. (1) Adaptation to local environments causes divergence among populations or related species occupying different regions. (2) Character displacement in response to competition for resources creates diversity among related species occupying the same region. (3) An elevated rate of speciation precludes gene flow between diverging groups, thereby coupling an increase in species number with growing phenotypic variety. When Dobzhansky, Lack, and Simpson originally proposed the concepts that comprise the Ecological Theory of adaptive radiation, they sought to explain patterns of diversity that they observed in contemporary faunas (all three being zoologists) or the fossil record, largely in the absence of empirical support for the central processes.
The primary goal of The Ecology of Adaptive Radiation is to assess evidence that has accumulated during the past half century concerning local adaptation, character displacement, and ecological speciation, thereby testing the Ecological Theory. In the first three chapters, Schluter delimits his perspective on adaptive radiation, describes four exemplary cases that satisfy his criteria, and reviews evidence concerning temporal patterns of adaptive radiations. The next five chapters comprise the core of the book, in which Schluter outlines the Ecological Theory of adaptive radiation and evaluates the evidence for its key components. Schluter then strays from his ecological emphasis to present a chapter reviewing recent developments in quantitative genetics that bear on diversification. The book closes with a final assessment of the Ecological Theory and Schluter's forecast for future developments in our understanding of adaptive radiation.
Despite the emphasis on the Ecological Theory, The Ecology of Adaptive Radiation is very much about empirical evidence. In describing the Ecological Theory, Schluter relies on verbal, conceptual description, rather than formal mathematics. Indeed, the most mathematical sections of the book address various statistical techniques for studying diversification, rather than the theory of radiation. For most of the topics that he considers, Schluter marshals empirical support broadly, drawing examples from microorganisms, plants, and animals. This evidence often involves vertebrates, largely reflecting the focus of studies of diversification processes, rather than a bias arising from Schluter's experience as a vertebrate ecologist. Through his contributions to the primary literature, Schluter has established a reputation for weighing evidence critically, and this care is also a distinctive feature of The Ecology of Adaptive Radiation. Overall, this book provides a detailed overview of the current state-of-play of studies of diversification, particularly those that bear on the Ecological Theory.
What audience Schluter had in mind while writing The Ecology of Adaptive Radiation is not obvious. Schluter has packed this book densely with both concepts and examples. Often, this density is achieved by limiting explanation, as though Schluter was constrained by a page limit imposed by the publisher. Consequently, the uninitiated reader will have difficulty understanding many important concepts without consulting supplementary sources (as became evident in a graduate seminar course that I lead based on The Ecology of Adaptive Radiation). In contrast, readers who are already familiar with the key ideas of diversification will find little new in The Ecology of Adaptive Radiation. Schluter relies entirely on concepts and examples drawn from the primary literature, and his synthesis of this information exposes few new perspectives on diversification. Thus, The Ecology of Adaptive Radiation provides a dense retrospective of the Ecological Theory of adaptive radiation, describing most of the central issues, relevant techniques, and convincing examples. By consolidating this information in a single source, The Ecology of Adaptive Radiation could invigorate interest in a fundamental problem in biology. It may also stimulate new questions and approaches as readers recognize that much remains to be learned about the diversity of life.
The scope of adaptive radiation
In his discussion of species diversification, Simpson (1953)
emphasized its variable tempo and extent, proposing that "[d]iversification may be brief or prolonged and may be of limited scope or may ramify into the most extraordinarily varied forms ...." (p. 223). At one end of this spectrum lies adaptive radiation, which Simpson characterized as "... more or less simultaneous divergence of numerous lines all from much the same ancestral type into different, also diverging adaptive zones" (p. 223). Given that adaptive radiation is an extreme in a continuum, what can we learn by studying it (or reading a book about it)? Is adaptive radiation merely a curiosity, or is it responsible for much of organic diversity?
Surprisingly, Schluter barely addresses these questions. In the preface, after listing three exemplary cases of adaptive radiation (including Hawaiian silverswords), Schluter asserts that "[m]uch of life's diversity, perhaps even most of it, has arisen during similar episodes of speciation and phenotypic and ecological divergence" (p. vii). Uncharacteristically, given his extensive use of empirical examples, Schluter offers no evidence to support this claim. Schluter returns to this topic only in the closing paragraphs of his book, proposing that the relative contribution of adaptive radiation to biotic diversity will be a central topic of the next half-century of research on diversification. It seems strange that a phenomenon of apparently uncertain significance has stimulated enough research to be reviewed in a 288-page book.
In part, the importance of adaptive radiation remains elusive because, as Simpson noted, it is one end of the diversification continuum, rather than the outcome of a discrete process. Thus, the prevalence of adaptive radiation depends on how restrictively it is defined. Schluter explicitly adopts a narrow conception to guide his evaluation of empirical evidence. Specifically, he considers that adaptive radiation occurs when populations speciate rapidly from a common ancestor in association with functional, phenotypic differentiation caused by divergent selection. This definition necessarily excludes investigation of ancient bouts of rapid diversification, such as the proliferation of angiosperms, because the link between trait utility and environment during the period of differentiation can no longer be demonstrated. Consequently, Schluter focuses on recent or ongoing radiations involving closely related species in the same genus. Not surprisingly, qualifying cases comprise a relatively short list, which is dominated by examples from geologically young and isolated "islands," especially the Galápagos and Hawaiian Islands, and the African rift lakes—examples that Simpson (1953
, p. 227) characterized as "radiation of a minor sort." Given such narrow circumscription, what can we learn about diversification in general? The answer seems to depend on whether interest focuses on conditions that initiate radiations or those responsible for continued, rapid divergence once diversification has begun.
Many of the examples considered by Schluter may not represent the circumstances that initiate an adaptive radiation on the continental and oceanic areas that support most of Earth's diversity. In his seventh chapter, Schluter reviews two situations that can initiate an adaptive radiation: ecological release and key innovation. Ecological release may be the norm for adaptive radiations on newly formed, isolated islands, because chance colonists confront extensive, unexploited ecological opportunities. As Schluter demonstrates (section 7.3), such opportunity can foster rapid speciation on islands, compared to that realized on a continent with an established flora and fauna. Ecological release was also probably widespread after the few mass extinctions that have punctuated the history of life on Earth (Simpson, 1953
). Regardless of its scale, ecological release is heuristically appealing because repeated instances may result in parallel patterns of adaptive radiation, which are amenable to the statistical comparative method promoted by Schluter.
Unlike the situation on young islands, adaptive radiations in continental and oceanic regions often occur within an established biota of competitors, predators, and mutualists, so they may seldom be precipitated by ecological release. Instead, radiation in established biotas may commonly start with the chance evolution of a phenotypic innovation (e.g., vascular tissue), which enables adaptive exploration of new ways of life. In the first instance, such key innovations likely require "key mutations" (Simpson, 1953
), starting an adaptive radiation with a random genetic event, rather than a repeatable ecological circumstance. Being unique, key innovations are largely unsuited to statistical analysis, because lack of replication precludes discrimination between alternate explanations. As a result, many key innovations are not amenable to the rigorous analysis that Schluter favors, regardless of their contribution to diversity. Nevertheless, if continental and oceanic radiation commonly begin with a key innovation, then studying ecological release on islands may provide limited insight into the initial conditions that sparked the adaptive radiations that created most biological diversity.
On the other hand, the cases that Schluter considers probably illustrate many of the general mechanisms responsible for diversification, whether during an adaptive radiation or during more gradual differentiation. Roughly two-thirds of The Ecology of Adaptive Radiation reviews local adaptation, character displacement, and ecological speciation, drawing support mainly from examples of species pairs that are not obviously associated with ongoing adaptive radiations. Indeed, the limited direct connection to adaptive radiation in the long chapter on local adaptation provoked several students in a graduate seminar and me to ask independently, "What is the point of this chapter?" The answer is that the mechanisms responsible for adaptive diversification apply generally, regardless of whether it occurs gradually or explosively during a radiation. The differences in tempo result from circumstance, rather than a change in the mode of evolution.
History as guide and constraint
Science, like natural selection, is an historical process in that new developments depend on the legacy of past generations. Reliance on precedent is constructive because it guards against repeated exploration of unsuccessful approaches. However, dependence on the past can also limit innovation. Both the virtues and constraints of history are evident in The Ecology of Adaptive Radiation.
In deference to the Ecological Theory, Schluter gives primacy to its central mechanisms, namely local adaptation, character displacement, and the establishment of reproductive isolation in association with adaptation. Schluter recognizes that diversification can result from other ecological and nonecological process, but he presents these mechanisms as extensions and alternatives to the Ecological Theory, so that they receive less attention. This approach will interest historians of ecological thought; however, it may also perpetuate historical biases, rather than fostering development of an integrated, inclusive perspective on the processes responsible for diversification.
Historical bias is manifest in Schluter's consideration of the processes responsible for species richness. The number of species representing a lineage at any time depends on the balance between speciation and extinction. Thus, species richness can increase because of a relatively high speciation rate or a low extinction rate, and it increases most rapidly when both conditions hold. Either case leaves more species, which may diversify phenotypically and functionally, resulting in an adaptive radiation. Perhaps even more than speciation, which can involve nonecological mechanisms, extinction is a purely ecological process that occurs when population death rate exceeds the birth rate for a protracted period. Furthermore, a low extinction rate unequivocally demonstrates adaptedness within a lineage. Given their joint role in diversity, both speciation and extinction deserve thorough discussion in a book that considers the ecology of adaptive radiation. However, Schluter admits to being "more interested in speciation than extinction" (p. 176), and he does not consider the causes of extinction or variation in extinction rates. In this omission, Schluter continues the emphasis on speciation of the Ecological Theory and reflects the prevailing perspective in evolutionary ecology, which considers population dynamics only superficially. The absence of an overview of extinction renders The Ecology of Adaptive Radiation incomplete as a review of the processes that govern diversity.
Schluter also perpetuates a bias of the Ecological Theory by limiting his definition of phenotype to morphology, thereby largely ignoring diversification in physiology (and behavior). For Simpson, this bias was understandable, both because he was a paleontologist and because during the 1950s physiologists did not adopt an evolutionary perspective. However, perpetuation of this emphasis is not justified, given recent developments in the study of evolutionary physiology (reviewed by Feder, Bennett, and Huey, 2000
). (Unfortunately, this trend has largely evaded plant physiology, as only 5.8% of projects currently funded by the NSF Program in Ecological and Evolutionary Physiology consider plant physiology from an evolutionary perspective.) By ignoring physiology, many cases of adaptive radiation that involve limited morphological divergence may go unrecognized. More importantly, consideration of physiology acknowledges that the competition responsible for divergent natural selection can involve both resource acquisition, the focus of Schluter's review, and the efficiency of resource use. For example, the main innovation preceding radiation of most of the major grass lineages is the independent evolution of C4 photosynthesis (Kellogg, 2000
), which enhanced rates of carbohydrate production in warm, open environments, such as tropical savannas. Examples such as this reveal the virtue of including physiology as an integral component of evolutionary diversification.
Surprisingly, given the historical motivation for The Ecology of Adaptive Radiation, Schluter does not elaborate on the central issues of past conceptual debates about key elements of the Ecological Theory. Notable examples include resource competition, character displacement, and reinforcement of incomplete reproductive isolation. These debates probably receive little attention because of space limitations and Schluter's apparent belief that they have been resolved by the weight of empirical evidence. Nevertheless, an overview of these previously contentious issues would have helped illustrate both the rationale for Schluter's insistence on empirical verification and the necessary and sufficient characteristics of evidence for adaptive radiation and its mechanisms.
Natural selection, life history, and adaptive radiation
Darwin (1859)
considered that natural selection occurs when individuals with dissimilar phenotypes differ genetically only with respect to either survival or gamete production. In contrast, Darwin distinguished selection based on differences in mating and/or fertilizing success, or sexual selection, from natural selection, because he recognized that sexual selection can favor traits that compromise survival. In The Ecology of Adaptive Radiation, Schluter follows Darwin's narrow conception of natural selection (although this perspective does not become evident until Chapter 8).
Since Darwin, understanding of fitness has evolved considerably, leading to a more general conception of natural selection, which places no limit on the types of fitness differences that cause phenotypic change (see Endler, 1986
) and so includes sexual selection as a special case. This inclusive conception of natural selection recognizes that fitness arises from the combined effects of all morphological, physiological, and behavioral traits on an organism's lifetime schedule of reproductive output. This chain of trait
life historyfitness bears several implications for the evolution of diversity. Because traits affect fitness indirectly via the life history, trait evolution must be accompanied by life-history evolution. Consequently, adaptive radiation must involve diversification of both traits and life histories. However, life-history evolution is strongly constrained by various trade-offs between life-history components (reviewed by Roff, 1992
; Stearns, 1992
). Therefore, the fitness value of alternate traits depends on their effects on all aspects of performance, including survival, gamete production, mating success, and fertilization success, so that natural selection (in the narrow sense) and sexual selection do not occur independently. Finally, because events that occur early in life affect fitness more strongly than those that happen late, adaptive radiation is more likely to involve either static traits that do not change during an organism's life or dynamic traits with greatest expression during early life stages.
In The Ecology of Adaptive Radiation, Schluter focuses on morphological diversification as the essence of adaptive radiation. Unfortunately, Schluter does not consider the life-history link between morphology and fitness directly, so that we learn little about life-history evolution during adaptive radiations. No doubt this omission reflects the absence of empirical analysis of life histories in the context of adaptive radiation. Nevertheless, given the governing role of life history in fitness, this central topic warrants exploration.
Morphological ecology and adaptive radiation of plants
Botanists may be inclined to dismiss The Ecology of Adaptive Radiation as being too zoological, because most examples involve animals (especially vertebrates). This reaction would be unfortunate, both because the concepts considered apply broadly and because the paucity of botanic examples conveys a clear message. Given the circumscribed scope of The Ecology of Adaptive Radiation, Schluter has reviewed the relevant botanical and zoological literature extensively (41 pages of citations) and he uses botanical examples freely when they are available. For example, Schluter uses plant examples exclusively to demonstrate the virtues of transplanting hybrids into parental environments to assess the scope of divergent selection, because this powerful technique has not been applied to animals. Thus, the underrepresentation of botanical examples largely reflects limited empirical analysis by botanists of the ecological processes that Schluter considers responsible for diversification.
Schluter explains that he presents relatively few botanical examples because demonstrations of "[s]traightforward relationships between phenotypes and resource use are scarce in plants ..." (pp. 145–146). By "phenotype," Schluter means morphology, and he ascribes the deficiency of botanical examples to the importance of physiology in the interaction of plants with their environments. However, this explanation cannot be complete, as plants exhibit remarkable morphological variation, which presumably evolved to serve more than the amusement of taxonomists. Indeed, as Niklas (1992
, p. 47) noted, "all plants share essentially the same metabolic machinery and compete for the same resources. Thus structural solutions to deal with the physical and biotic factors in their environments have become paramount in their ecology and evolution."
I see two reasons why Schluter could find few examples of the correspondence between plant morphology and environment to illustrate his perspective on adaptive radiation. First, relatively few studies of plant morphology consider its ecological function (although see Niklas, 1992
) and those that do typically do not incorporate the approaches needed to demonstrate adaptation in natural conditions. Consider the structure of flowers and inflorescences, the most morphologically diverse organs produced by plants. Despite long-standing recognition that many aspects of the structure of these organs serve pollination, experimental demonstrations of functions of specific floral traits are few. As a consequence, most descriptions of the roles of specific aspects of flower and inflorescence structure remain little more than "just-so" stories. That most of Schluter's botanic examples involve floral characteristics illustrates that the functions of nonreproductive organs have received even less experimental attention. Thus, the relation between plant morphology and ecological function offers many opportunities for future exploration, whether in the context of understanding morphological diversity or motivated by interest in how plants work.
The second factor limiting botanical examples for Schluter's review is the rarity of studies of functional morphology that incorporate explicitly evolutionary perspectives. For a radiation to be adaptive, trait diversity must arise by divergent natural selection that creates functional differences between related taxa. Consequently, relevant studies must compare trait function in related species, an approach seldom implemented in botanical studies. Much additional insight into diversification can be gained from experimental studies that attempt to recreate ancestral phenotypes, by physical manipulation, hybridization, or artificial selection, and then contrast their performance with that of contrasting descendant phenotypes (e.g., Schemske and Bradshaw, 1999
). Unfortunately, studies of plant structure seldom include experimental, comparative analysis of function, so we remain largely ignorant of the purpose of morphological diversity.
Consider the Proteaceae, a southern hemisphere family of 
1000 species, which exhibits a bewildering variety of both vegetative and reproductive morphology. For example, among the roughly 340 Australian species of Grevillea are species named buxifolia, pinifolia, pteridifolia, and quercifolia, because their leaves resemble those of boxwood, pine, fern and oak, respectively. The function of these differences in leaf form remains unexplored and unknown. Abetted by this lack of comparative, functional analysis, the Proteaceae continues the elusive ploy of its namesake, the Greek sea god Proteus, who assumed different forms to avoid answering questions. The Ecology of Adaptive Radiation provides a detailed overview of many approaches that could be applied in overcoming such protean evasion in any lineage.
Lessons learned
Schluter concludes The Ecology of Adaptive Radiation claiming that "[t]here is little doubt that the (ecological) theory (of adaptive radiation) will continue to serve as the starting point for new investigations into the dramatic episodes of speciation and differentiation that have generated much of the ecological diversity on earth" (p. 243). The Ecological Theory is destined to serve this role, both because of historical inertia and because it explains many features of biotic diversity. However, the Ecological Theory is not complete. Schluter acknowledges this by including a chapter on the quantitative genetics of selection, thereby deviating from a purely ecological explanation. In addition, Schluter correctly notes that "... speciation remains the least understood part of adaptive radiation" (p. 212) and, in my preceding comments, I have identified other components that warrant attention. Perhaps the time has come to acknowledge gratefully the contributions of the Ecological Theory, but to abandon its biases and work toward an inclusive theory of diversification.
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FOOTNOTES |
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2 Phone (403-220-6489), FAX (403-289-9311), (harder{at}ucalgary.ca
).
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LITERATURE CITED |
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TOPINTRODUCTIONLITERATURE CITED |
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Endler J. A. 1986 Natural selection in the wild. Princeton University Press, Princeton, New Jersey, USA
Feder M. E. A. F. Bennett R. B. Huey 2000 Evolutionary physiology. Annual Review of Ecology and Systematics 31: 315-341
Kellogg E. A. 2000 The grasses: a case study in macroevolution. Annual Review of Ecology and Systematics 31: 217-238[CrossRef][ISI]
Niklas K. J. 1992 Plant biomechanics: an engineering approach to plant form and function. University of Chicago Press, Chicago, Illinois, USA
Roff D. A. 1992 The evolution of life histories; theory and analysis. Chapman and Hall, New York, New York, USA
Schemske D. W. H. D. J. Bradshaw 1999 Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proceedings of the National Academy of Sciences, USA 96: 11910-11915
Simpson G. G. 1953 The major features of evolution. Columbia University Press, New York, New York, USA
Stearns S. C. 1992 The evolution of life histories. Oxford University Press, Oxford, UK
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