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Paleont. 21, 172 (2001). London B. Biol. Sci. 275, 47 (2008). 10.1126/science.1157719 REVIEW tion of an underpopulated area (e. g., island or lake), extinction of previously ecologically dom- on February 7, 2009 inant groups, or evolution of a character— Adaptive Radiation: sometimes termed a “key innovation”—that allows the lineage to interact with the environ- Contrasting Theory with Data ment in novel ways (1, 2). Different evolutionary factors allowing the populations to take advan- Sergey Gavrilets1* and Jonathan B. Losos2 tage of new ecological opportunity have been em- phasized, including genetic drift in small founder Biologists have long been fascinated by the exceptionally high diversity displayed by some or peripheral populations (9), relaxed (9) or strong evolutionary groups. Adaptive radiation in such clades is not only spectacular, but is also an selection (2, 10), and hybridization (11, 12). www.sciencemag.org extremely complex process influenced by a variety of ecological, genetic, and developmental factors and strongly dependent on historical contingencies. Using modeling approaches, we Empirical Approaches for Studying identify 10 general patterns concerning the temporal, spatial, and genetic/morphological Adaptive Radiation properties of adaptive radiation. Some of these are strongly supported by empirical work, whereas Four main empirical approaches have been used: for others, empirical support is more tentative. In almost all cases, more data are needed. Future Fossils. Methods based on fossil data allow progress in our understanding of adaptive radiation will be most successful if theoretical and one to infer the history of the clade through time empirical approaches are integrated, as has happened in other areas of evolutionary biology. and to use information from extinct taxa. The disadvantages of this approach are incomplete- Downloaded from he spectacular diversity of life on Earth include Darwin’s finches on the Galápagos is- ness of the fossil record, difficulty in assessing the that Darwin sought to explain in On the lands, Anolis lizards on Caribbean islands (Fig. 1), adaptive significance of phenotypic variation among TOrigin of Species emerged through a va- Hawaiian silverswords, and cichlids of the East taxa, and the absence of ecological, behavioral, riety of intricate biological processes. One of African Great Lakes (Fig. 2), among many others physiological, and other types of data. these is adaptive radiation, which some consider (1, 2, 6). Phylogenetic comparative methods. Phylo- of foremost importance and potentially responsi- Adaptive radiation has two components: the genetic approaches take advantage of increas- ble for much of the ecological and phenotypic production of new species (speciation) and the ingly complete phylogenies for many important diversity of life (1, 2). “Adaptive radiation” refers adaptation of constituent species to a diversity of groups and have the ability to integrate studies of to those evolutionary groups that have exhibited ecological niches. Although many classic adapt- the evolution of organismal function and ecology. an exceptional extent of adaptive diversification ive radiations are both species rich and adaptively The main disadvantage of these methods is that into a variety of ecological niches (2–4), with disparate (7), this correlation is far from perfect: extinct taxa are often not represented so that there such divergence often occurring extremely rap- Some adaptive radiations have relatively low spe- is no way, for example, to detect whether a clade idly (5). Classic examples of adaptive radiation cies richness (e.g., Darwin’s finches, Australian has been more species-rich in the past. Moreover, pygopodid lizards); alternatively, some speciose phylogenetic inferences about character states in 1Departments of Ecology and Evolutionary Biology and clades contain little adaptive disparity and thus the past can be unreliable (13, 14). Mathematics, National Institute for Mathematical and Biolog- would not qualify as adaptive radiations (3, 8). Microevolutionary studies of extant taxa. ical Synthesis, University of Tennessee, Knoxville, TN 37996, 2 The classic view of adaptive radiation focuses Studies focusing on traits of and processes affect- USA. Museum of Comparative Zoology and Department of — Organismic and Evolutionary Biology, Harvard University, 26 on ecological opportunity, in which an ancestral ing extant taxa e.g., phenotypic characters, eco- OxfordStreet,Cambridge,MA02138,USA. species finds itself in an environment in which logical niches, spatial structure, genetics, local *To whom correspondence should be addressed. E-mail: resources are abundant and underutilized. Such adaptation, competition, and sexual selection— [email protected] resource availability may result from coloniza- can elucidate much about the processes driving 732 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org SPECIALSECTION tion are allopatric, parapatric, and sympatric, cor- responding to zero, intermediate, and maximum migration, respectively (19–21). Alternatively, mechanisms of speciation can be classified accord- ing to biological mechanisms driving divergence and speciation, e.g., random drift, ecological se- lection, or sexual selection (23, 24). However, sometimes very different biological mechanisms have underlying dynamic common- alities and therefore can be described by very sim- ilar mathematical models. Therefore, classifying mechanisms of speciation and adaptive radiation on the basis of similarity of the corresponding models can be more general and insightful than on the basis of particular biological factors. Five partially overlapping sets of models can be identified. In “spontaneous clusterization” models, an initially random mating population accumulates a substantial amount of genetic var- iation by mutation, recombination, and random drift and then splits into partially or completely reproductively isolated groups [reviewed in (20)]. Spontaneous clusterization models describe the accumulation of Dobzhansky-Muller genetic in- compatibilities, speciation by hybridization, di- on February 7, 2009 vergence in mating preferences, or allochronic Fig. 1. Adaptive diversification in Caribbean Anolis lizards. On each island in the Greater Antilles, anoles have speciation (i.e., speciation via divergence in the diversified to produce the same set of habitat specialists. Shown here (clockwise from top left) are A. cybotes, timing of life-cycle events related to reproduc- trunk-ground specialist, Hispaniola (photo: J. Losos); A. pulchellus, grass-bush, Puerto Rico (photo: J. Losos); tion). In “invasion of empty niches” models [e.g., A. insolitus, twig, Hispaniola (photo: L. Mahler); A. chlorocyanus, trunk-crown, Hispaniola (photo: M. Losos). (25, 26)], a few founders enter a new environment with a number of novel discrete ecological niches. adaptive radiation and sometimes even include has emerged over the past 40 years [reviewed in As selection acts on the new genetic variation manipulative experiments. However, extrapola- (19–21)], has clarified many questions and topics supplied by mutation, different lineages become tion from processes operating today to what hap- hotly debated by generations of biologists.