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Accounting for Biological Diversity1

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Accounting for Biological Diversity1 BOOK REVIEWS Evolution, 57(5), 2003, pp. 1216±1220 ACCOUNTING FOR BIOLOGICAL DIVERSITY1 DOUGLAS J. FUTUYMA Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109-1048 Received March 7, 2003. design, statistical rigor, analytical invention, and appreciation The concept of adaptive radiation (or at least the term) was of natural history that he has brought to his studies of stick- fathered by D. Lack, G. G. Simpson, and other contributors lebacks and geospizine ®nches (which, appropriately, are to the Evolutionary Synthesis, and re¯ected their conviction among the frequently cited examples). He is often suitably that most evolution, including differences among species, tentative in his conclusions, describes alternative hypotheses, was caused by environmental agents of natural selection. If and points out enough unexplored issues to provide inspi- that were true, and if cladogenesis often occurs in bursts of ration for countless doctoral dissertations (or research ca- almost simultaneous diversi®cation (as inferred by paleon- reers). Indeed, I can report that his book is an ideal basis for tologists and supported by the proli®c polytomies in many modern molecular phylogenies), then adaptive radiation, graduate student seminar courses, and can both educate and which Dolph Schluter de®nes as ``the evolution of ecological spark spirited discussion. These strengths abundantly out- diversity within a rapidly multiplying lineage,'' would ac- weigh whatever reservations may attach to some few of count for much of the boundless diversity of species and their Schluter's arguments. characteristics. In assessing the prevalence and causes of adaptive radiation for the ®rst time since the Synthesis, Schlu- General Patterns ter addresses as great, as encompassing, a theme as biology An immediate problem is how to distinguish adaptive ra- sounds. diations from other forms of diversi®cation, such as non- The ``ecological theory'' of adaptive radiation that devel- adaptive radiation, or diversi®cation in which speciation oped during the Synthesis, Schluter notes, was tripartite: di- events are prolonged through time rather than clustered. vergence between species is caused by different selection (Such problems of distinction and measurement plague many owing to differences in the species' habitats and resources; aspects of the study of adaptive radiation; for example, mak- evolution of differences in habitat and resource use is driven ing meaningful distinctions among resources to compare diet by competition or permitted by alleviation of competition; breadth or ``niche breadth'' can be very dif®cult [Colwell speciation (the evolution of reproductive isolation) is a con- and Futuyma 1971].) Schluter describes several ways of de- sequence of the divergent natural selection that drives phe- tecting ``rapid speciation,'' but does not use them to deter- notypic and ecological differentiation. At least through the mine if any real clades are or are not instances of adaptive 1950s, the theory was based mostly on patterns described by radiation. Curiously, he requires that members of an adaptive paleontologists and systematists, and quantitative studies radiation differ in ecologically important morphological or were few. Since then, population genetic models, phyloge- physiological characters; groups of species such as MacAr- netic analyses, experimental studies of form and function, thur's famous warblers, that differ in resource use only by ecological studies, and quantitative genetics have been virtue of their behavior (surely a phenotypic trait), are ex- brought to bear on the elements of the theory, as well as on cluded. more recent ideas pertaining to adaptive radiation. Schluter A more serious issue, I think, is the very important pos- sets out to reevaluate the theory in the light of modern studies, sibility that species in many clades may constitute ``non- concentrating on diversi®cation at low taxonomic levels (e.g., adaptive radiations,'' in part or in whole, in which ecological within genera). He concludes that ``[o]n the whole, it should differences are minimal, or may have evolved well after spe- be regarded as one of the most highly successful theories of ciation. Among herbivorous insects, for example, there are evolution ever advanced'' (p. 242). But as he ably describes, many potential examples (cf. Ross 1957). In the skipper ge- much of the theory's support is based on only a few well- nus Erynnis, for instance, many sympatric host-specialized studied cases and we do not know how far they can be gen- species feed on the same species of oaks (Burns 1964). The eralized. The role of factors other than divergent ecological possibility of undetected ecological differences cannot be selection and competition is poorly understood, and some ruled out, but the burden would seem to fall as heavily on profoundly important questions are still virtually without an- the advocates of Gause's axiom as on its skeptics. Schluter swer. recognizes this problem, especially when he discusses ``non- Schluter's treatment of this grand subject is marked by the ecological speciation'' (see below), but he treats ecological same consciousness of hypothesis-testing and experimental differences among related species much more extensively than possible cases of the contrary. We are left without any 1 The Ecology of Adaptive Radiation. Dolph Schluter. 2002. Ox- estimate of what fraction of cladogenetic events are associ- ford University Press, Oxford and New York, viii 1 288 pp. HB ated with ecological divergence. $85.00, ISBN 0-19-850523-X; PB $45.00, ISBN 0-19-850522-1. Of particular interest is Schluter's analysis of possible 1216 q 2003 The Society for the Study of Evolution. All rights reserved. BOOK REVIEWS 1217 trends within adaptive radiations. He concludes, in agreement as four million years. This is an increasingly active area that with long-term patterns in the fossil record, that expansion yields diverse and sometimes surprising results. For instance, of a clade's breadth of habitat or resource use is the most intraspeci®c phenotypic variance-covariance matrices may general feature of adaptive radiations. He compiles phylo- predict interspeci®c divergence patterns better than genetic genetic studies to probe the long-standing hypothesis that matrices do (Baker and Wilkinson 2003). Such long-term ecological generalists give rise to specialists more often than correspondence between intraspeci®c and interspeci®c vari- the reverse (i.e., specialization is relatively irreversible). ation has the important implication that developmental path- Schluter concludes that, at least at low taxonomic levels, there ways are so structured as to constrain the expression of ge- is no evidence of a bias in direction, and specialization is netic variation over long time spans, and provides an alluring not an impediment to ecological diversi®cation. (As an in- interface between population genetics and macroevolution. dication of how rapidly phylogenetic analyses are informing The postulated agent of phenotypic divergence in adaptive our understanding of such issues, Nosil [2002] has summa- radiations is divergent selection, under which, according to rized a considerable number of studies of host range evolution Schluter, intermediate phenotypes have lower ®tness. He in phytophagous insects that have been published even since abundantly employs Wright's adaptive landscapes (or, more Schluter's analysis; he largely supports Schluter's conclu- often, R. Lande's analogue for quantitative traits), so that sion.) It is nevertheless the case that many clades remain divergence entails shifts to new adaptive peaks. This is ®ne limited to a rather narrow adaptive zone for many millions if the peaks are dictated by discrete resources to which dif- of years (e.g., insect clades restricted to a single host-plant ferent phenotypes are best suited, but becomes problematical family, swifts restricted to foraging for ¯ying insects), so an when competition impels character divergence; if a contin- ecological version of Dollo's law may sometimes hold at a uum of character states (e.g., gape size) are best suited to a truly macroevolutionary scale. Schluter also draws attention continuous array of resources (e.g., prey sizes), there need to ``replicate radiations'' as evidence of predictability in not be ®tness valleys, except insofar as these are generated adaptive radiation. Despite considerable attention to conver- by density-dependent and frequency-dependent selection, in gent community structure during the optimistic days of which case the landscape metaphor becomes less useful (as ``MacArthurian'' community ecology (e.g., Orians and Sol- Schluter notes). With or without density-dependent selection, brig 1977; Orians and Paine 1983), examples are few, and the critical assumption is that each phenotype zi has a resource counterexamples might perhaps have been given more atten- (or habitat) optimum ri, that is, that phenotypes display trade- tion. For example, Lack (1969) pointed out that six species offs in ®tness on different resources. Under this assumption, of tits (Paridae) coexist in Europe, whereas no more than two a jack of all trades is master of none, and we should often species (now assigned to different genera) are typically sym- expect the evolution of ecological specialization, and indeed patric in most of North America. The cases of parallel ra- the inde®nite proliferation of increasingly specialized species diation (e.g.,
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