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Adaptive Radiation ADAPTIVE RADIATION Rosemary G. Gillespie,* Francis G. Howarth,† and George K. Roderick* *University of California, Berkeley and †Bishop Museum I. History of the Concept ecological release Expansion of habitat, or ecological II. Nonadaptive Radiations environment, often resulting from release of species III. Factors Underlying Adaptive Radiation from competition. IV. Are Certain Taxa More Likely to Undergo Adap- founder effect Random genetic sampling in which tive Radiation Than Others? only a few ‘‘founders’’ derived from a large popula- V. How Does Adaptive Radiation Get Started? tion initiate a new population. Since these founders VI. The Processes of Adaptive Radiation: Case carry only a small fraction of the parental popula- Studies tion’s genetic variability, radically different gene VII. The Future frequencies can become established in the new colony. key innovation A trait that increases the efficiency with GLOSSARY which a resource is used and can thus allow entry into a new ecological zone. adaptive shift A change in the nature of a trait (mor- natural selection The differential survival and/or re- phology, ecology, or behavior) that enhances sur- production of classes of entities that differ in one or vival and/or reproduction in an ecological environ- more hereditary characteristics. ment different from that originally occupied. sexual selection Selection that acts directly on mating allopatric speciation The process of genetic divergence success through direct competition between mem- between geographically separated populations lead- bers of one sex for mates or through choices made ing to distinct species. between the two sexes or through a combination of character displacement Divergence in a morphological both modes. character between two species when their distribu- sympatric speciation The process of genetic diver- tions coincide in the same ecological environment gence between populations occupying the same geo- compared to overlap of the character in question in graphic range leading to distinct species. the two species when they are geographically sepa- taxon cycle The repetitive pattern by which wide- rated. spread dispersive stage I populations or species give convergence The evolution of similar characters in ge- rise to more restricted and specialized stage II popu- netically unrelated or distantly related species, often lations or species; subsequent divergence leads to as the result of selection in response to similar envi- stage III local endemics. ronmental pressures. Encyclopedia of Biodiversity, Volume 1 Copyright 2001 by Academic Press. All rights of reproduction in any form reserved. 25 26 ADAPTIVE RADIATION Numerous definitions of adaptive radiation have been in isolation, without any ecological change. This may proposed. Almost all incorporate the idea of diversifi- lead to patterns of considerable genetic distance be- cation in ecological roles, although they differ in their tween morphologically similar species from different emphasis on relative rates of proliferation. Here, we isolates (Schneider and Moritz, 1999). Similarly, diver- propose a definition that seeks to be general but at sification of snails on islands has frequently been the same time removes any implication of process: attributed to topographical isolation [e.g., Crete Adaptive radiation is a pattern of species diversification (Gittenberger 1991) and Medeira (Cameron et al., in which different species within a lineage occupy a 1996)]. In general, it appears that (i) nonadaptive diversity of ecological roles, with associated adapta- radiation occurs if there is isolation without any novel tions. ecological opportunity and (ii) coexistence of species within a lineage will not occur in nonadaptive radia- tions but is a primary characteristic of adaptive radia- I. HISTORY OF THE CONCEPT tions. Beginning with the work of Darwin (1859) on the Gala- pagos fauna, the concept of adaptive radiation, in terms of diversification of ecological roles by means of natural III. FACTORS UNDERLYING selection, has been recognized. The term was first used ADAPTIVE RADIATION by Osborn (1902) in describing parallel adaptations and convergence of species groups on different landmasses. The common requirement for triggering adaptive radi- Subsequently, it was developed as a major tenet for ation is the opening up of ecological space. This may arguments presented in the modern synthesis by Huxley be allowed by intrinsic factors, i.e., something that (1942). Simpson (1953), working on paleontological changes in the organism to allow radiation to occur; data, discussed the importance of key innovations in for example, evolution of tolerance toward noxious triggering adaptive radiation. For a detailed history of plant chemicals (Farrell and Mitter, 1994; Mitter et the concept of adaptive radiation, see Givnish (1997). al., 1988). Alternatively, it may occur as a result of Much recent information has been added, particularly extrinsic factors; for example, it has been reported during the past decade with the rise of molecular meth- to occur in geological history after an influx of ods (Givnish and Sytsma, 1997). nutrients into the system (Vermeij, 1995), in recent evolutionary time when new islands are colonized (Wagner and Funk, 1995; Liebherr and Polhemus, II. NONADAPTIVE RADIATIONS 1997), and in ecological time when a new habitat opens (Rainey and Travisano, 1998). The term ‘‘nonadaptive radiation’’ has been used to For ancient radiations, it is often difficult to deter- describe situations in which species proliferation has mine the relative importance of intrinsic and extrinsic not been attended by diversification of ecological roles factors in allowing adaptive radiation. Factors associ- (Gittenberger, 1991). When proliferation is simply a ated with such radiations include (i) coincidence (after consequence of isolation, with isolated sibling species a slight delay) with major extinction episodes (Sloan maintaining similar ecological affinities, then the radia- et al., 1986) and (ii) radiation of a group frequently tion cannot be considered ‘‘adaptive.’’ As will be starting from a small, unimpressive set of species from described later, isolation has been invoked to explain an earlier period. For example, fossil ammonites the initial divergence of taxa in some radiations (e.g., (shelled cephalopod mollusks) reveal episodes of tre- Galapagos finches and cichlid fish), with the adaptive mendous proliferation and extinction through the Dev- phase not occurring until recently diverged sibling onian, Triassic, Jurassic, and Cretaceous (Fig. 1; Leh- species become sympatric. However, there are some mann, 1981). Echinoderms show a similar pattern, cases of nonadaptive radiation, with many allopatric originating in the Ordovician and undergoing small and ecologically similar species. Most of these radia- radiations until all but one lineage went extinct by the tions are caused by changes in topography that, instead end of the Permian (Smith, 1984). These then radiated of opening up new habitats, have served simply to extensively in the Triassic–early Jurassic, and the cur- isolate a previously more widespread species. For rent diversity of forms remains similar to what arose example, isolated mountaintops and other continental at that time. refugia have allowed species long periods of evolution The great placental radiation (Ͼ4300 species) has ADAPTIVE RADIATION 27 FIGURE 1 The differentiation of the ammonoids from the Devonian to the Cretaceous, based on the number of genera. Strippled area, new genera; Hatched area, continuous genera. From Lehmann, 1981, reprinted with the permission of Cambridge University Press. been attributed partly to the extinction of many reptil- A. Intrinsic Factors: Key Innovations ian groups at the end of the Cretaceous (Simpson, 1953). The parallel adaptive radiation of marsupials in Simpson (1953) suggested that the evolution of a suite Gondwana has also been attributed to the Cretaceous of traits, or key innovations, that increase the efficiency extinctions and subsequent opening of ecological space with which a resource is used might allow species to (Springer et al., 1997). However, within each lineage enter a ‘‘new’’ adaptive zone, and the ecological opportu- (placentals and marsupials) key innovations may have nity thus allowed might promote diversification. The been involved: The radiation of ungulates and rumi- concept of the key innovation is an essential element nants is associated with the opening up of the savannas in hypotheses of the evolution of specialization and (Fig. 2) but would not have happened if the organisms subsequent adaptive radiation in herbivorous insects. did not develop the morphological and physiological However, the nature of key innovations is not often features necessary to exploit the habitat. Similarly, the clear. In an attempt to define more clearly the concept, radiation of the diprotodontians appears to have com- Berenbaum et al. (1996) examined cytochrome P450S menced in the Eocene and may have been promoted and its relation to the adaptive radiation of butterflies. by a key adaptation for herbivory (Springer et al., 1997). They found high levels of diversification in substrate The actual basis for radiations subsequent to extinction recognition sites between species that do not share the episodes is still a subject of debate, particularly because same set of host plants; the reverse was true for those coincidence between extinction events and subsequent species that do share host plants. This
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