Luke J. Harmon,1,2,3 Jonathan B. Losos,4 T. Jonathan Davies,5 Rosemary G. Gillespie,6 John L. Gittleman,7 W. Bryan Jennings,8 Kenneth H. Kozak,9 Mark A. McPeek,10 Franck Moreno-Roark,11 Thomas J. Near,12 Andy Purvis,13 Robert E. Ricklefs,14 Dolph Schluter,2 James A. Schulte II,11 Ole Seehausen,15,16 Brian L. Sidlauskas,17,18 Omar Torres-Carvajal,19 Jason T. Weir,2 and Arne Ø. Mooers20
1 2

Department of Biological Sciences, University of Idaho, Moscow, Idaho 83844 Biodiversity Centre, University of British Columbia, Vancouver, BC V6T1Z4, Canada

E-mail: lukeh@uidaho.edu

4 5

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 National Center for Ecological Analysis and Synthesis, University of California, Santa Barbara, 735 State Street, Suite 300,

Santa Barbara, California 93101
6 7 8 9

Department of Environmental Science, Policy and Management, University of California, Berkeley, California 94720 Odum School of Ecology, University of Georgia, Athens, Georgia 30602 Department of Biological Sciences, Humboldt State University, Arcata, California 95521 Department of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, St. Paul, Minnesota 55108 Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 Department of Biology, Clarkson University, Potsdam, New York 13699 Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520 Division of Biology, Imperial College London, Silwood Park Campus, Ascot, SL5 7PY United Kingdom Department of Biology, University of Missouri—St. Louis, St. Louis, Missouri 63121 Institute of Ecology & Evolution, Division of Aquatic Ecology & Macroevolution, University of Bern, CH-3012 Bern,

10 11 12 13 14 15


Eawag Centre of Ecology, Evolution and Biogeochemistry, Department of Fish Ecology & Evolution, Seestrasse 79,

CH-6047 Kastanienbaum, Switzerland
17 18 19 20

National Evolutionary Synthesis Center, Durham, North Carolina 27705 Oregon State University, Department of Fisheries and Wildlife, 104 Nash Hall, Corvallis, Oregon, 97331 ´ Escuela de Biolog´a, Pontificia Universidad Catolica del Ecuador, Apartado 17-01-2184, Quito, Ecuador ı Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A1S6, Canada

Received May 11, 2009 Accepted February 21, 2010


C 2010 The Author(s). Journal compilation Evolution 64-8: 2385–2396


2010 The Society for the Study of Evolution.

However. Here. H A R M O N E T A L . identifying adaptive radiations has proven difficult due to a lack of broad-scale comparative datasets. and African lake cichlids. 1992. Some of these focus on lineage accumulation (e. Methods We obtained dated phylogenies and body size and shape measurements for 49 clades of animals. We applied a phylogenetic comparative approach to test Simpson’s model and investigate the dynamics of phenotypic evolution across the history of clades. see many chapters in Givnish and Sytsma 1997).g. Butler and King 2004. The clades spanned a wide range of species richness and each corresponded to an easily recognizable taxon (e. O’Meara et al. Givnish 1999.. almost all accepted adaptive radiations come from endemic radiations of species on isolated oceanic islands or lakes (e. Across our entire analysis. Schluter 2000. and return to the relationship between the tempo of lineage diversification and that of morphological evolution in the discussion. as ecological space becomes filled. Grant and Grant 2008. were commonly supported. When lineages first enter these zones. The youngest clades appear to evolve most rapidly because long-term change typically does not attain the amount of divergence predicted from rates measured over short time scales. and the historical relationships of species summarized in a phylogenetic tree. Hendry and Kinnison 1999.. Simpson defined adaptive radiation as “more or less simultaneous divergences of numerous lines from more or less the same ancestral adaptive type” (Simpson 1959). criteria for recognizing adaptive radiations are murky (but see Givnish 1997. George Gaylord Simpson famously postulated that much of life’s diversity originated as adaptive radiations—more or less simultaneous divergences of numerous lines from a single ancestral adaptive type. including Hawaiian Tetragnatha spiders. Kinnison and Hendry 2001.g. 2006). which is more closely related to Simpson’s (1944) model in which organisms diversify upon entering new adaptive zones (Losos and Miles 2002).L U K E J.g. the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. Foote 1994. and famously postulated that much of life’s diversity originated during these adaptive radiations. McPeek 2008. Rabosky and Lovette 2008. Simpson’s adaptive zones represent sets of similar niches that are ecologically available to a particular lineage and free from potential competitors. clade age. may be rare in comparative data. We compared the fit of this model to both single selective peak and random walk models. KEY WORDS: Adaptive radiation. we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation. Phillimore and Price 2008. Most previous studies of evolutionary rates have used comparisons of characters at the beginning and end of a given time interval (Gingerich 1983. calculated as the average age to maturity among all species for which data were available.. phylogeny. identifying adaptive radiations has proven difficult due to a lack of broad-scale comparative datasets. 1953) who brought the idea to the forefront of evolutionary biology. Baldwin and Sanderson 1998. in which initially rapid morphological evolution is followed by relative stasis. Recent analyses indicate a prevalence of early rapid accumulation of lineages followed by a slowdown in net diversification through time (Nee et al. In fact. model fitting. Although the concept of adaptive radiation traces back to Henry Fairfield Osborn (1902). the EB model in which evolution is fastest early in a clade’s history and slows through time. the rate of morphological evolution should then slow (Simpson 1944. Linder 2009).g. Gillespie 2004. We found little support for the early-burst model of adaptive radiation. We created larger trees for some analyses by combining individual trees within major taxonomic groups. we found that the net rate of morphological evolution varied inversely with clade age. Brownian motion. Anolis lizards.. In addition. Several theories predict how adaptive radiation might proceed (see Schluter 2000). We develop this approach further here. We refer to this as the “early burst” (EB) model. The goal of our study was to test a particular pattern of adaptive radiation. comparative methods. it was George Gaylord Simpson (1944. Seehausen 2006. 2003. Our dataset included several a examples of clades commonly recognized as adaptive radiations. across a large comparative dataset. We suggest that the classical model of adaptive radiation. Recent advances in phylogenetic comparative methods have opened new approaches to reconstructing the temporal dynamics of evolution when time series are not available (Martins 1994. We focus here on the tempo and mode of morphological evolution. Galapagos finches. 2001. Gal´ pagos finches). These methods rely on two types of information: the distribution of phenotypes of contemporaneous species in a given group. particularly that of selective peaks. where morphological evolution is initially rapid and slows through time. Felidae). Harmon et al. Schluter 2000). However. This table also provides the estimated generation time of individuals within each clade. method of phylogenetic tree construction. morphological evolution should initially be rapid. whereas both other models. Estes and Arnold 2007). Beyond these systems. Details of sample size. Blomberg et al. and body size data are summarized in Table 1. and their prevalence in the tree of life uncertain. many of which were geographically localized (e. grafting the 2386 EVOLUTION AUGUST 2010 . Losos 2009). 2003).

84 0.3 16 5 58.10 0. Chamaeleonidae 5. Piranga 24.04 0 Clade n n in tree Clade age (million years) Tree building method Gen.26 0. We also list the maximum likelihood estimate of the net rate of body size evolution (σ 2 ) see Supporting Information Appendix Tables 2 and 3 for other parameter estimates. Phelsuma 8.13 0.61 0.00 0. Poecile 25.65 0.09 0.25 0. .14 E A R LY B U R S T S O F E VO L U T I O N A R E R A R E EVOLUTION AUGUST 2010 13 18 15 15 13 27 12 7 10 7 20 11 16 14 14 13 23 12 6 10 6 16 8.84 0.73 0. Passerina 23. Details of sample size.51 0.31 0.43 0.72 0.17 0. Icteridae 2 § (South American) 15.26 0.03 0 0. Ocyalus. Muscisaxicola 22.12 0.30 1.09 0.97 0.14 0.22 0.40 0. We also list the Akaike weights for the BM. This table also provides the estimated generation time for each clade. Psarocolius.17 0.08 0.17 0. Icterus 21. Pygopodidae 10.17 0.08 0.31 0.29 0.42 0. Iguaninae 6.0‡ 5.82 0.6 12 12 24 TarL † TarL TarL † TarL12. Icteridae 1 ♦ (North American) 14.6 60 12 37.14 0.07 0.16 0.16 0.84 0.94 1 EB 0 0.41 2.04 0.33 0.59 0. SSP.75 0.13 0.22 0.13 0.63 0.511 15.71 0. and body size data.73 0.Table 1. Phrynosomatinae 9.19 0.08 0.09 0.2 12 18 19.58 0.09 0.00 0.21 0.) 3. Corytophaninae 4.03 0.67 0.30 0.43 0.05. clade age.22 0.41 0. Catharus 16.3 7. Group BM 0.5‡ Bayes+PL 18 MandL 179 73 9 29 9 67 20 70 31 29 38 19 10 118‡ 401 65‡ 94‡ 65‡ 74‡ 6.01 0.11 SSP EB BM 0 0.25 0.14 18 15 8. Varanus 12.08 0. and Cacicus Continued.58 0.0‡ 8.59 0.31 0. Liolaemini 7.7‡ ML+PL ML+PL2 ML+PL ML+PL4 ML+PL ML+PL ML+PL5 ML+PL ML clock7 ML+PL8 ML+PL9 Bayes+PL Bayes+PL 9. Alcidae 13.16 0.08 0.66 0.02 0.23 0.17 0. The rate of evolution for one clade (Vermivora) could not be estimated because differences among species are smaller than the expected variation due to measurement error alone.09 0.81 0.84 0. Empidonax 18.16 0.02 0.21 0. and EB models for body size and shape for all clades with at least 10 species.15 0.75 0.67 1.10 0.14 0 0.00 0. Bold indicates the model with the highest AIC weight.66 0.02 0.8‡ 8.1‡ 2.82 0.49 0.20 0.70 1 0.08 1.17 0. Gruinae 20.69 0.67 0. Chlorospingus 17. this dataset was excluded from further analyses.45 0.09 0.58 0.16 0. calculated as the average age to maturity among all species for which data were available.32 0.9‡ Bayes+PL Bayes+PL Bayes+PL UPGMA11 Bayes+PL14 Bayes+PL Bayes+PL Bayes+PL Bayes+PL Bayes+PL Bayes+PL 12 12 18 12 48. Anolis (Carib.13 √ 3 Mass14 TarL † MandL TarL † TarL † TarL † TarL † 0.74 2387 1.16 0.32 0.08 0. Agamidae 2. Clypicterus.3‡ 8.89 0.5‡ 10.43 0.59 0.20 2. Stenocercus 11.59 0.4‡ 8.09 0.6 75‡ 37‡ 41‡ 112‡ 10‡ 7.74 0.8‡ 4.14 0.29 0.12 0.14 1.70 0.45 0.61 0.74 0.17 0.27 0.46 0.8 63 18 SVL SVL3 SVL SVL SVL SVL SVL5 SVL SVL7 SVL SVL10 TarL † TarL † 0. Geospizini 19.72 0.2 0.17 0.09 0.74 0.10 0.03 0.0‡ 7. method of phylogenetic tree construction.01 0 Squamates Birds 381 150 9 161 36 204 44 125 38 61 62 24 19 0.14 0.53 0.4 24 6 12. time (months) Size variable Rate of body size evolution Body size AIC weights Body shape AIC weights SSP 1 0.

25 √ 3 √Mass 3 √Mass 3 √Mass 3 √Mass 3 Mass √ 3 √Mass 3 Mass SVL28 0.926 19. Xiphorhynchus 33. 18 Joyce et al. 2003.15 0. H A R M O N E T A L . age based on molecular calibration from fossil data. 2001. Desmognathus 47 34 23 44 30 23 5227 18.48 0. 2005.20 0. Quiscalus. 25 Gillespie 2004. L U K E J. Enallagma 40. 2005.00 0. Sylvia 29. Etheostomatinae 39. 4 Townsend and Larson 2002. 2005. 2006.19 0. Qgelaius.58 0.20 0. . Cichlids (South African Rivers) 36.64 0.8 0.01 0.2‡ 15−17 24.01 6 10 162 76 16‡ ML+clock 9 SL 7 3. 15 Near et al.11 1. 3 Harmon et al.99 2.99 0.0‡ 12. Oreopsar.30 0. 2005. ‡. 20 Near and Keck 2005.57 0. Cichlids (East African Rivers) 37.60 0.218 9 ML+clock18 SL18 5.427 18 12 12 8 14.3‡ 5.5‡ 6. Toxostoma 31. 5 Harmon et al.25 5 5.Table 1.4 16. Vermivora 32.54 0.22 0.70 0. 12 Lack 1947.38 6 3. Felidae 44.6 38 122 12 7 62 33 36 62 31 89 30.17 0.01 0.818 9 2.59 0.00 0. 19 Page et al. ♦ includes Dives.13 0.57 0. Lampropsar. Ramphocelus 28. 14 Mooers et al.51 0.87 211. Pseudoleistes. 2005. Mustelidae 45. Canidae 43. § includes Gnorimopsar.15 0.00 0.00 0.426 32.62 2.96 0 0. Continued.08 0. and Scaphidura. 17 Near et al.99 0.37 0. Chrysomus.819−21 1022 722 24.99 0.47 0.13 0.60 0.20 0.2 TarL † TarL † TarL † TarL † TarL † TarL † TarL † SL15−17 SL18 0. 6 Austin et al. 2005. Gymnomystax. 2008. †. Herpestidae 46.9‡ 5.79 0.56 0.25 Supertree26 Supertree26 Supertree26 Supertree26 Supertree27 SL19−21 √ 3 ∗∗22 √Mass∗∗22 3 Mass TL24. Euphagus.00 0. Cichlids (Lake Tanganyika) 38.13 Arthropods 0 0.5 24.82 3.00 0.0‡ 8.25 0. 16 Collar et al. 8 Torres-Carvajal et al.23 0.18 0. mass of final instar.00 0. ∗∗. Molothrus.12 EVOLUTION AUGUST 2010 Fish 20 8 22 8 10 7 17 20 22 0. Tachycineta 30.0‡ 7.08 0.56 1.09 0. 2388 Group BM 0. Lestes 41. 23 Stoks et al.23 0. 22 Turgeon et al.15 0.15 0.16 0. References: 1 Shochat and Dessauer 1981. 10 Pepin 2001.60 0 0. 2 Nicholson et al.31 Clade n n in tree Clade age (million years) Tree building method Gen.99 0 0.16 0 1.78 0. tarsus length also used.00 1.03 0 0 Mammals 200 42 16 62 34 36 65 37 97 Supertree27 Supertree26 Bayes+PL28 19. 11 Petren et al.20 0. Ptilonorhynchidae 27. 9 Ast 2001.64 0. and Macroagelaius.20 0 0 Amphibians 26.21 0. .2 59 Bayes+PL19−21 ML+clock22 ML+clock23 UPGMA24.07 0. 1999. unpublished data. 26 Bininda-Emonds et al. 2003.926 17.51 0.21 0. 2003.21 1. time (months) Size variable Rate of body size evolution Body size AIC weights EB Body shape AIC weights 0. 24 Gillespie et al. 1994. Primates (Old World) 47.21 0.56 ML+clock18 SL18 11 6 17 7 6 6 15 20 17 14. Strepsirrhini 48.60 0.11 SSP EB BM SSP 0. Cichlids (Lake Makgadikgadi) 35. Curaeus. new ML phylogeny prepared. 7 Jennings et al. 2005.126 2028 ∗. 2003. 2004.58 0. Tetragnatha 42.99 0. Viverridae 49.2 24. Agelasticus. 28 Kozak et al.20 0.526 13.55 6.17 0.00 0.20 1 0.29 0.4518 Bayes+PL Bayes+PL Bayes+PL Bayes+PL Bayes+PL Bayes+PL Bayes+PL Bayes+PL15−17 ML+clock18 45 12 12 12 12 12 18 36 9 0.18 0. 13 Grant and Grant 2002. 21 Near and Benard 2004.09 0.18 0. Xanthospar.61 0. 27 Vos and Mooers 2006. Agelaioides. Centrarchidae 34. 2007.72 0.1 15.

Under each of the three models (BM. and S is a matrix whose elements sij are described above. Because we were interested in comparing net rates of body size evolution. corrected for sample size (AICc. Freckleton and Harvey 2006). This model ¯ has four parameters: z o .org/). or (when only two characters were measured) by obtaining the residuals from a regression of a log-transformed trait on the log-transformed body size measurement. σ2 . Each set of tip values has a likelihood: L= exp −1 2[X − E(X)] (V)−1 [X − E(X)] (2π) N · det(V) . where sij are the elements of a matrix S representing the shared path length from the root to the common ancestor of taxa i and j and σ2 is a parameter describing the rate at which taxa diverge from each other through time (Felsenstein 1973. the net rate parameter. Principal component loadings and the proportion of the total variance explained by PC2 are available in the Appendix (Table S1).. 2007). the crown age of each clade) from literature or unpublished data (Table 1). we also generated a body shape axis by performing a principal components analysis on the correlation matrix of a set of log-transformed measurements. We obtained an independent axis of body shape by retaining the second axis (PC2). σ2 . Table 1). and EB). We restricted r to values below zero to correspond with a model in which net rates decrease through time.. a parameter representing the ancestral state value for the clade. We did not have enough samples within species to estimate this standard deviation from our data.datadryad. Vos and Mooers 2006. this model reduces to the BM model. This model is equivalent to BM if α = 0. SSP. and the model reduces to three parameters. Finally. V is derived from the expectation under an Ornstein–Uhlenbeck model of evolution. although for reasonable parameter values. However. by taking the cube-root of mass) and log-transformed. we use an average value calculated across 210 taxonomically varied animal species (0.” bearing in mind that the dispersion of phenotypes under a random-walk model is different from one in which traits change directionally through time (Bookstein 1987). For the SSP model. when fitting an SSP model to comparative data with ultrametric trees. and prime ( ) denotes transpose. Hugall et al. Data are available on Dryad (http://www. Blomberg et al. the ancestral state. the strength of the constraint moving trait values back toward the optimum. We compared fits of three different models to each dataset using the Akaike information criterion. Under the BM model. Hansen 1997. In all of these datasets. we standardized these data by dividing by an estimate of the average within-species standard deviation in body size. θ. Our statistical approach has sufficient power to distinguish among these three models for moderately sized phylogenetic trees. and α. For most clades (39 of 49). We also estimated the absolute age of the root node of each tree (i. Sugihara 1978): a random walk (BM. These data were converted to a linear scale where necessary (e. the estimated ancestral state for the clade. T is the time of the deepest split in the tree. such that trait values have a tendency to return to a medial value (SSP. 2003. the initial value for the net rate parameter. Expected tip values follow a multivariate normal distribution with an expected ¯ mean vector E(x) = z o . modeled as Brownian motion). 2003. although eight of the trees were derived from supertree analysis and two using Unweighted Pair Group Method with Arithmetic Mean (UPGMA.0772. and an EB model in which the net rate of evolution slows exponentially through time as the radiation proceeds (EB. BinindaEmonds et al. see also Ackerly 2009). there are two parameters. r (3) ¯ This model has three parameters: z o . o and r. Instead. power to detect the EB model is much lower than power to detect the SSP model (see Appendix). and has elements (Hansen 1997. V determined by the model and phylogenetic tree. expected tip values follow a multivariate normal distribution with an ex- pected mean vector E(X) and covariance matrix. Most phylogenies were constructed using maximumlikelihood or Bayesian analysis of molecular gene sequence data. the trait optimum.e. modeled as an Ornstein–Uhlenbeck process. under the EB model. 2007. the maximum-likelihood ancestral state and trait optimum are equal. We refer to this parameter as an estimate of evolutionary “net rate. when r = 0. We also compared the fit of the three models to various subtrees and supertrees constructed from our data (see Results). a random walk with a single stationary peak (SSP). Butler and King 2004) Vij = σ2 −2α(T −sij ) e (1 − e−2αsij ) 2α (2) where σ2 and α are the net rate and constraint parameters of the model. and an expected covariance matrix V. a parameter describing the pattern of rate change through time. We calculated branch lengths using fossil age calibrations and either a strict or relaxed molecular clock (Table 1). modeled as a BM process with a timedependent dispersion parameter.g. McKellar and Hendry 2009). N is the number of species. with elements V ij = σ2 sij .E A R LY B U R S T S O F E VO L U T I O N A R E R A R E phylogenies onto chronograms from recent studies of tetrapod diversification (Vitt et al. 2003) Vij = 0 sij 2 2 σo er t dt = σo er sij − 1 . V has elements (Blomberg et al. PC1 provided an index of body size and was strongly positively correlated with all original character axes. Butler and King 2004). (1) where X is a vector of phenotypic values for the species in the tree. We compiled a variety of indices of body size for species in each clade from museum specimens or previous literature (Table 1). EVOLUTION AUGUST 2010 2389 .

1988). see also Harmon et al. more inclusive clades (Fig. 2. evolution resembling an OU model on an SSP can be produced when both natural selection toward an optimum and random drift act on a phenotypic character (Lande 1976. When we pooled the results for each model across datasets by multiplying the likelihoods across all trees. and greater variation under the SSP model. A hypothetical phylogenetic tree of four species is depicted. 2003). We also computed model-averaged parameter estimates following Burnham and Anderson (1998). whereas EB predicts that young subclades. We focus on one simple implementation in which net rates of morphological change decline exponentially through time. SSP predicts that young subclades will capture much of the variation in trait values and thus be approximately as variable as older. for example. whereas blue circles indicate the amount of variation in the whole clade. and computed the Akaike weights for each. Because our implementation of the EB model is new. as would be produced by. we used a search algorithm to find maximum-likelihood parameter values for each clade. but a substantial number favored an SSP model (body size: 12/38. Felsenstein 1988). pygopodid lizards). we found very strong support for the SSP model for Figure 1. or when neutral evolution takes place in a tightly constrained part of morphospace such that trait values are limited to a certain range. the main difference between the SSP and EB models relates to the expected variance in trait values of young subclades within each higher clade. We consider some alternatives in the Appendix. one might impose a constraint parameter that becomes stronger through time. There are a number of ways one might model such a process. All three models are compatible with a range of evolutionary processes. Table 3. We also analyzed the data assuming other levels of measurement error. Similarly.0345 on a natural log scale. will exhibit less variation than older.63.0772. Conceptually. increasing interspecific competition as niches become filled. better than the BM or SSP models. For a given phylogenetic tree size. SSP (single stationary peak). such that rates near the tips are overestimated (Martins 1994). these analyses did not qualitatively affect our results. 25/38.61. The length of each red line at the tips of each tree indicates the magnitude of a given morphological character for each species. Green circles indicate the amount of variation within subclades in the tree. see also Appendix Tables 2 and 3). Fig. Varanus lizards. Subclades have much lower variation under the EB model. body shape. 0. This model is meant to be a general model of increasing constraints on evolutionary change through the course of an adaptive radiation. 14/29).L U K E J. body shape. when each is contrasted to the BM model. diversifying at the end of a presumed radiation. SSP. or one might allow deep clades in a phylogenetic tree to have separate optima. Results Analysis of individual clades showed that the time course of morphological evolution differ substantially among clades. For example. Maximum likelihood estimate of model parameter values and. We present results based on a standard error equal to 0. For all three tested models. Measurement error can cause a significant bias in evolutionary rate reconstructions. although body shape appears to be constrained more often than body size (Table 2). 1. 2390 EVOLUTION AUGUST 2010 . 2006). body shape. 14/29. Any of these models would fit data that showed rates that slow through time. within which there are strong constraints. for clades with at least 10 species. representing the expected error for sample size of five individuals per species given an average within-species standard deviation of 0. To account for this effect. the Akaike weights for the BM. BM: body size. Example illustrating the differing predictions for the BM (Brownian motion). H A R M O N E T A L . BM can result from both genetic drift and directional selection where the direction of selection fluctuates randomly through time (Felsenstein. we will discuss it in more depth. 0. and EB models mostly supported a BM model (Tables 2 and 3. Only two datasets showed weak support for the EB model (Fig. 2. regardless of the form of that slowdown. For example. Results were roughly similar across body size and shape. more inclusive groups. maximum Akaike weight: body size. one has less power to detect EB when it is the true model of evolution compared to SSP (see Appendix). We then compared the overall fit of these three models to the entire body size and shape dataset by calculating the product of the likelihood of each model across all trees. we modeled measurement error directly by adding variation to the diagonal of the expected among-species variance–covariance matrix (O’Meara et al. and EB (early burst) models of morphological evolution.

n=1484. were generally very small (body size. mean α = 0.4 −780.7 205. mean α = 1. SSP was always favored (57 cases. the parameter from the EB model that describes the rate at which trait evolution slows through time. The lack of EB patterns might be due.8 27.9 13.5. n=1094) and various taxonomic subsets. for r.0 AICBM 134.4 27.5 −781. insect.6 −1496. but when there was strong support for a single model (Akaike weight > 0.4 −369.0 3. some overlapping).2 84. we could not estimate parameters for the SSP model because the likelihood surface exhibited a flat ridge (see Butler and King 2004).6 EVOLUTION AUGUST 2010 2391 . We count both the number of clades with the highest AICc values for a particular model (“maximum w”) and those with weights greater than 0.0 −327. BM Clades All Squamates Birds Fish Insects Mammals Amphibians Phenotype Body size Body shape Body size Body shape Body size Body shape Body size Body shape Body size Body shape Body size Body shape Body size Nc 49 39 11 11 21 20 6 5 3 1 7 2 1 Np 98 78 22 22 42 40 12 10 6 2 14 4 2 lnL −3696.9 72. we considered both smaller subsets and larger combinations of our focal clades. body shape. range: 0–8.6 −66.0 AICC 0 0 0 0 7. and Np the number of parameters.7 −66.6 −853.1 157.95 (“w>0. in part. 41 clades. body shape: 103/205) or SSP (body size: 61/284.9 −280. range: −0.0 39. bird. body shape: 99/205) over the EB model (body size: 10/284.9 12. When we fit models to all subclades within trees with 10 or more species from every tree (body size: 284 subclades.2 −421. mammal.5 −438.6 0 SSP Np 147 117 33 33 63 60 18 15 9 3 21 6 3 lnL −3580. shape: 39 phylogenies.34.0 −369.1 52.95”). Table 2). most clades favored BM (body size: 215/284. fish.E A R LY B U R S T S O F E VO L U T I O N A R E R A R E Table 2.2 −748. Excluding those datasets.95 BM 25 0 14 0 215 0 103 0 SSP 12 6 14 8 61 21 99 36 EB 1 0 1 0 10 0 5 0 All subclades Body size Body shape both body size and shape across almost all the major taxonomic groups (amphibian. body shape: 5/205).5 −437. Nc gives the number of clades.6 −59. 42 clades. Higher lnL and lower AIC values indicate better model support. mean r = −0.00032–10. see Appendix).95).5 −780. body shape.5 −190.4 −729. range: −0.6 −1483.9 −280.6 −60.3 −174.2 6.6 0 0 23.9 −184. 35 clades.1 19.9. mean σ2 = 0.95 Maximum w w>0. In some cases.0 −268.8 145.55.9 132.9 54.3 0 2.3 −136. range: 0. see Appendix). mean r = −0. Model-averaged estimates Table 3. 42 clades.0071. To address this problem.3 −172. Clades All full clades Dataset Body size Body shape Number of phylogenies 49 39 284 205 Criterion Maximum w w>0.0036.5 −851. for each model.2 0 0 0 0 1.0 12. Model-averaged parameter values varied widely across datasets but showed the same general pattern.3 AICEB 220.15 to 0.041 to 0.95 Maximum w w>0. expressed as the expected variance in trait means per million years in units of within-population standard deviations.0 −651.5 39.0 EB Np 147 117 33 33 63 60 18 15 9 3 21 6 3 lnL −3690.95 Maximum w w>0. we found a range of modelaveraged estimates for the net rate parameter σ2 (body size.9 23. or squamate) in our dataset (Table 3). range: 0–20. to our choice of focal clades.5 −191.0 −729.7 2. results were consistent.4 −60. Number of clades and subclades with n>10 species showing support for each of the three models (BM.1 −1493.6 0.2 11. SSP.74. the best-supported model is in bold.0 −66. body shape 205 subclades. When we analyzed body size evolution Results of model fitting tests combining likelihoods across all clades (size: 49 phylogenies. see Appendix) and the constraint parameter α (body size. 33 clades. and EB) for body size and body shape. body shape net rate parameter estimates are unit dependent and cannot be compared.2.5 0 44.

insect. Akaike weights for three models of phenotypic evolution (BM. Relative area of the bar filled with any color is proportional to the Akaike weight for that model given the data. the net rate of body size evolution was faster in the younger clades. 3). Table 4). The slope of this relationship did not vary significantly within each group of nonbird higher taxa (amphibian. mammal. Numbers correspond to the datasets as listed in Table 1. early burst. carnivores. the best predictor of net evolutionary rate is crown clade age (the age of the most recent common ancestor of all living species). H A R M O N E T A L . the term adaptive radiation is sometimes used to describe evolution that occurs at a fast net rate. fish.98). single stationary peak. We have represented one particular pattern predicted to result from adaptive radiation with our EB model. primates) did not support any one model (all Akaike weights < 0. Fig. Because our data mix several kinds of measurements and our analyses compare net rates across different time intervals.01 from simulations described in the Appendix. not applicable because shape data were unavailable) for all phylogenetic trees in the dataset. Brownian motion. P < 0.6.” only birds supported the EB model (Akaike weight = 0. Although some clades appeared to be evolving more quickly than others.66).38. we limit our rate comparisons to body size because comparing net rates of body shape evolution across clades is problematic due to differing scales of measurement). which demonstrate that our patterns are robust and are not a statistical artifact of our methods. EB.80. Figure 2. Fig. NA. summarized in the Appendix.L U K E J. If EB-like patterns 2392 EVOLUTION AUGUST 2010 . or squamate. Indeed. whereas the other two major clades (squamates. with the oldest groups showing the slowest net rates of evolution (r = −0. SSP. Body size in most bird clades evolved slowly compared with other clades of the same age (Fig. regardless of whether that rate slows through time. we carried out a series of analyses. in combined trees made by pasting individual trees together by taxonomic group into larger “supertrees.01 from simulations described in the Appendix. estimated net rates of body size evolution of clades under a BM model spanned four orders of magnitude (Fig. Birds were the only group that did not show such a relationship. Excluding birds from the analyses strengthened the negative relationship between net rate and age (r = −0. 3). weakly supported the SSP model (Akaike weight = 0. Another of these large trees. 3. see Appendix). Discussion We find surprisingly little evidence for the EB model of morphological change in our comparative datasets. P < 0. 3). however.

Gray circles represent bird clades.71 α 0. Lande (1976) described a model in which a population evolves on a constant adaptive peak and.38 0. it is often the case that young pairs of sister species are still morphologically very divergent. under the SSP model. Relationship between clade age and average rate of body size evolution. very few clades show patterns of rapid morphological evolution followed by relative stasis.21 EVOLUTION AUGUST 2010 2393 . Higher AIC weights indicate better support of the model from our data. phenotypic evolution follows the pattern described by our SSP model. to correspond with the relatively large values of α estimated for our comparative data (see Appendix).20 1. or both.57 0.71 Akaike weight 0. and the strength of stabilizing selection in Lande’s (1976) model.45 0.74 phenotypic standard deviations per million years.05 0 0 0 0 Akaike weight 0. These two parameters describe the net rates of evolution over short (σ2 ) and long (α) time scales (Hansen 1996.2 × 10−6 phenotypic standard deviations per generation (using the range of generation times.53 0. Using this mean. with the thin black line including birds and the thick red line excluding them.92 0. we find that net rates of phenotypic change are too fast over short time scales (high estimated σ2 ) but too slow over long time scales (large estimated α) to be explained by long-term Table 4.03 0 Akaike weight 0.20 1. suggesting that the adaptive zone occupied by these species is not saturated. Model-averaged parameter estimates for our SSP model can thus be compared to empirical estimates of population size. with all other clades as red triangles.25 0.12 0. and represent the expected variance in body size accumulated per million years. Lines are least-squares regressions.71 r −0. Although our groups include many classic adaptive radiations. Our model-averaged value for the net rate of body size evolution is 0.59 1. Under this model.93 0.1 × 10−7 − 3. one would expect to detect them in a dataset of this size even given the relatively low power of this test (see Appendix). were common across the tree of life.001 0. Hansen and Martins 1996).54 1. Results of model fitting tests within various combined supertrees. In other words.54 1.92 0. and so one would need either very small effective population sizes (<10) or extremely strong stabilizing selection.31 1.004 0.98 0.012 0.5 months). Under a purely neutral model of genetic drift. this net rate is compatible only with very large Ne (∼300. Typical values of ω2 in the wild range from 3 to 50 with a mode of around 3 (Estes and Arnold 2007).4 (a typical value for morphological characters. we calculate an average net rate of σ2 ≈ 1. much higher than the typical range for species in the wild (∼10–100.32 0. over time.E A R LY B U R S T S O F E VO L U T I O N A R E R A R E Figure 3. σ2 ≈ 3. Estes and Arnold 2007).53 0. σ2 = h 2 /Ne and α = ω2 /2Ne (Lande 1976) where ω2 is the strength of stabilizing selection.009 0. heritability. traits seem to be evolving too slowly to be explained by a purely neutral model of genetic drift.7 × 10−6 ). phenotypes evolve according to a BM model with per-generation variance σ2 ≈ h2 /Ne where h2 is trait heritability and Ne effective population size (Lande 1976). Thus.59 SSP σ2 0.09 0. Model Phylogenetic tree Birds Squamates Mammals Carnivores Primates n 236 554 325 192 133 BM σ2 0. Assuming that heritability for body size across these species is 0.000. Rates were calculated using maximumlikelihood under a Brownian motion model. It is possible that this particular pattern is not a necessary part of adaptive radiation.003 0.21 EB σ2 74. Within classic adaptive radiations. Estes and Arnold 2007).66 0. The average generation time of our clades ranges from roughly five months to five years (mean = 20. When any of our datasets strongly supported a single model. it was typically a model of strong constraints.6 0.000).16 0. This suggests that radiations characterized by “EBs” of morphological evolution followed by slowdowns are rare.

Instead. the dynamics of trait evolution varied substantially among clades (Figs. rapid change is only apparent in young clades. but over a longer time interval. Harmon et al. however. Butler and King 2004. even among clades that represent some of the most cherished examples of adaptive radiations. Another recent study showed a clear pattern of decreasing rates of change through time of skeletal characters in early tetrapod evolution (Ruta et al. 2003). 2006). Despite the overall support for constrained models. Roopnarine 2003. although we find support for constrained models of evolution. our results suggest the provocative conclusion that EBs followed by slowdowns are genuinely uncommon across a broad portion of the tree of life. Hendry and Kinnison 1999. Siepielski et al. Kinnison and Hendry 2001. the model of adaptive radiation as a transient burst of morphological evolution at the base of a clade followed by stasis is rare. one large clade (all birds) strongly supported the EB model and showed patterns of body size evolution consistent with adaptive radiation (see also Starck and Ricklefs 1998). models invoking stabilizing selection around a single stationary peak require very weak selection. Under the SSP model. stabilizing selection of the magnitude typically estimated in field studies. we also ignored phylogenetic uncertainty in calculating evolutionary rates (O’Meara et al. 2006). 2001. species in older clades show similar amounts of change as species in younger clades. Our finding of high net rates of evolution over short time scales agrees with previous results from a wide range of data sources (Stanley 1975. Estes and Arnold 2007). An approach that combines direct historical information from fossils with phylogenetic information could increase statistical power. we considered only the evolutionary divergence of extant taxa based on their phylogenetic relationships. Estes and Arnold 2007). and similar model-fitting approaches can be used for fossil data (e. This pattern stands in contrast to recent results suggesting that slowdowns in lineage diversification through time are common in comparative data (McPeek 2008. 2005. For the traits and phylogenetic trees considered here. However. Our results suggest that a model of constant-rate BM. Hunt 2006). Lynch 1990. 2001. Phillimore and Price 2008. For example. H A R M O N E T A L . unrealistically small population sizes. Ruta et al.L U K E J. that such periods may be quite rare. Because of this. Rabosky and Lovette 2008). such that rapid evolution over short time scales is often counteracted by reversals (Gibbs and Grant 1987. For example. or perhaps because such “EBs” are genuinely uncommon across the tree of life. to interspecific comparative data. rather than direct historical information from fossils. such as Caribbean anoles. but the pattern is obscured by constraints on evolution over long time scales. 2 and 3). Alternatively. It is possible that evolution involves long periods of constraint punctuated by brief periods of directional selection (Gould 2002. and is consistent with the support in many of our clades for the SSP model. In this study. In our analyses. and thus have lower apparent net rates of evolution. Additionally. Thus. constraints on phenotypic evolution provide a potentially unifying explanation for the patterns we observed.. This is because our estimates of net rate effectively divide the amount of change by the time interval for that change. This could be because we have a nonrandom sample of trees. Hunt 2006. Gould 2002). Although our SSP model should capture some of the dynamics of these nonstabilizing selection constraints. Despite these caveats. Gal´ pagos finches. the effects of constraints on the overall amount of change are most apparent over long time periods. Future work could investigate differences among taxa or traits in the tempo and mode of evolution. Our broad-scale comparative dataset shows clearly that additional mechanisms are required to explain patterns of long-term stasis (Hansen 1997). fits some clades poorly. 2394 EVOLUTION AUGUST 2010 .g. but stabilizing selection over a species’ entire range appears to strongly constrain long-term evolutionary trajectories (Eldredge et al. Future work requires the application of more complex models. such that groups with a larger proportion of sympatric species early in their history might more likely exhibit an EB pattern of adaptive radiation as species interact and coevolve while filling ecological space (Schluter 2000. and East African a cichlids. developmental biology and genetics have revealed multiple instances of constraints directing evolutionary change (Barton and Partridge 2000. fossils are rare or absent from many clades suspected of recent adaptive radiation. 2006). Estes and Arnold 2007). Fossils can provide estimates of evolutionary rates (Gingerich 1983. and can explain the common observation of rapid evolution over short time scales and slower change over geological time scales (Eldridge et al. This contrast between patterns of lineage diversification and the accumulation of morphological disparity through time is worthy of future research. oscillating selection might be common in natural populations. assumed by most comparative methods. Gingerich 1983. a factor that could be incorporated into future work. Foote 1994). Fitting models that include explicit dynamics of populations evolving on adaptive landscapes might help to resolve this issue (Estes and Arnold 2007). the parameter estimates of the SSP model do not seem to match what is known about actual microevolutionary processes. 2005). or both. and might reveal more details about the dynamics of trait evolution in these clades (Polly 2001. because “EBs” do not leave a long-term signal in patterns of trait distributions across extant species. such as the peak-shift models described in Estes and Arnold (2007). Another possible mechanism involves the interaction between natural selection and the complex geographic structure of species: new trait values can evolve quickly within local populations. 2009). the amount of range overlap among species likely influences diversification. our results suggest.

———. J. Baldwin. T. G. L. J. ———. J. J. 1997. Kato. and L. F. J. C. Biol. Molecular evolution and adaptive radiation. Paleobiology 31:133–145. D. Natl. 1997. Larson. Foote. and the State of California. E. and J. Ecol. the University of California. P. Princeton Univ. D. Brakefield. Butler. Press. and diversification of the Hawaiian lobeliads. Rates of evolution on the time scale of the evolutionary process. J. F. T. 2002. Press. NY. Lande. King. Hansen. 640 pp. A. 2003. Linder. D. The pace of modern life II: from rates of contemporary microevolution to pattern and process.. A. E.. Santa Barbara. Nature 435:288– 298. B. Donnellan. 1987. J. dispersal. A. Plant species radiations: where. Endler. 2009. and diversification rates in dusky salamanders (plethodontidae: Desmognathus). Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales.. 354 pp. Natl. Fisher. H. R. Price. Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Systematics of the lizard family Pygopodidae with implications for the diversification of Australian temperate biotas. Acad. Mol. Cambridge. Am. Limits to natural selection. 2004. R. Evolution 57:717–745. Harmon.. A. Sytsma. Ives. Reid. R. S. N. G. Cambridge. Kinnison. 1464 pp. H. The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma). and P. Hum. R. 19:445–471. G. Acad. P. C. Cambridge. 2009. Cladistics 17:211–226. M. D. Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene Islands. R. 169:227–244. P. Grenyer. B.. Felsenstein. T. and K. R. M. R. Hagey. Syst. 272 pp. The dynamics of evolutionary stasis. Sci. M. 1997. Harvey. Sturmbauer. Alroy. Am. Beck. Adaptive radiation. C. D. J. Hendry. D. L. Nat. J. USA 91:2290– 2294. Lenski. Wagner for insightful discussions. Turner. R. 2005. B.. 4:e373. NESCent (NSF EF-0423641).. K. S. Soc. Jablonski. Univ. community structure. Genet. Acad. Joyce. B. 1–54 in T. and J. 2005. E. Hunt. J. Gittleman. S. J. R. P. An extant cichlid fish radiation emerged in an extinct Pleistocene lake. J.. of California Press.. P. 1947. S. A. Mitochondrial DNA evidence and evolution in Varanoidea (Squamata). Barton. a Center funded by NSF (EF-0553768). Purvis. Syst. 2000. 2006. Losos. Freckleton. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. 57:562–573. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Syst. C. R. N. 1986. Natl. Evolution 30:314–334. Harmon. 2004. Press. Jackson. 2007. Comparative analysis of morphological diversity: does disparity accumulate at the same rate in two lineages of centrarchid fishes? Evolution 59:1783–1794. Jochimsen. and A. Princeton. Press. eds. S. T. Princeton Univ. Rev. 2001.. McPeek. Kinnison. 1998. BLS was supported by a postdoctoral fellowship from the National Evolutionary Synthesis Center. Detecting non-Brownian trait evolution in adaptive radiations. Arnold. and S. A. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). T. and A. Givnish and K. 1930. R. Harvard Univ. Evolution 53:1637–1653. E. J. Phylogenet. T. USA 95:9402–9406. Gillespie. Larson. Phylogenies and quantitative characters. Trans. A. Evolution 51:1341–1351. why? Philos. Near. R. Proc. Cambridge Univ. Vos. J. Sci. S. Lunt. J. Berkeley. Bonett. 2001. 2006. F.. New York. Collar. Givnish. Gibbs. T. 2009. Maximum-likelihood estimation of evolutionary trees from continuous characters. Gavtilets. 164:683–695. LITERATURE CITED Ackerly. Katongo. J. Martins. B 363:3092–3105. Morphological disparity in Ordovician-Devonian crinoids and the early saturation of morphological space. Ann. C. 2007. The structure of evolutionary theory.E A R LY B U R S T S O F E VO L U T I O N A R E R A R E ACKNOWLEDGMENTS We wish to thank A. 25:471–492. Bills. J. Larson. Grant. Seehausen. 2004. R. Oscillating selection on Darwin’s finches. Systma. A. Jennings. 1996. and A. Nature 327:511–513. Am. J. B. P. Stabilizing selection and the comparative analysis of adaptation. Givnish.. Proc. NJ. Croom. D. Hansen. Springer-Verlag. Blomberg. P. and P. 1973. M. Nature 446:507–512. L. L. The delayed rise of present-day mammals. P. and M. F. Lieberman. Community assembly through adaptive radiation in Hawaiian spiders.. M. D. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. H. Adaptive radiation and molecular systematics: issues and approaches. Paleobiology 20:320–344. Nat. and M. Grant. H. J. M. Genetica 112–113:145–164. Ast. Paleobiology 32:578–601. K. Thompson. Melville.. 2002. Losos. Gould. A. B.. ———. Lond. B. Biol. Evol. Lack. and L. M. Sanderson. Kozak. The pace of modern life: measuring rates of contemporary microevolution... H. Givnish. Duftner. G. D. PLoS Biol. when. Gingerich. Natural selection in the wild. Unpredictable evolution in a 30-year study of Darwin’s finches. 2005. Cambridge Univ. Random walk and the existence of evolutionary rates. 2003. 2008. and A. R. 1999. Garland. Jones. 52:757–780. The biology of biodiversity. NJ.. Press. Gillespie. R. 2008. Harmon. A. J. Phylogenetic analysis of ecomorphological divergence. J. Sci. Tokyo. Bininda-Emonds.. L. N. 1987. D. Palumbi. N. 1994. O. J. J. T. E. Darwin’s Finches. Miller III.. How and why species multiply: the radiation of Darwin’s finches. R. and W. and E. Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. N. 1988. and P. R. 31:109–122. Molecular evolution and adaptive radiation. C. BioEssays 22:1075–1084. J. Paleobiology 13:446–464. and four anonymous reviewers provided helpful comments. A. Clarendon Press. J. Grant. Natural selection and random genetic drift in phenotypic evolution. B. Schulte II. Science 303:356–359. Rosenblum. Larson. Science 222:159–161. and S. 67–90 in M. ed. R. B. Partridge. Tempo and mode of evolutionary radiation in Iguanian lizards. Eldredge. M. Fitting and comparing models of phyletic evolution: random walks and beyond. Science 296:707–711. R. 2005. P. Cardillo. T. P. J. Wainwright. Pp. 512 pp. Hendry. Oxford. Princeton. Proc. Arnold. E. 1976. Press. EVOLUTION AUGUST 2010 2395 . and B. G. Pianka. Evolution 50:1404–1417. Uyeda. and C. Jones. N.. Losos 2003. T. and S. Bookstein. Cambridge Univ. and O. The genetical theory of natural selection. Science 301:961– 964. Rates of evolution: effects of time and temporal scaling. Austin. H. Genetica 112–113:127–144. M. Pp. A. AOM is supported by an NSERC Discovery Grant. This work was conducted as a part of the Adaptive Radiations Working Group supported by the National Center for Ecological Analysis and Synthesis. eds. W. Estes S. 1983. J. R. Arnold. G. MacPhee. A. CA. 318 pp. J.. 2001. 1994. USA 106:19699–19706. and P. Alfaro. Evolution 59:2000–2016. 1999. Multiple origins of a spider radiation in Hawaii.

. M. Nat. and M. D.. Ricklefs. Ricklefs. and A.. T. Price. Benard.. Physiol. eds. Rapid initial diversification followed by decrease in rates of character change. Proc. J. and T. A. 32:929–938. O’Meara. How humans differ from other animals in their levels of morphological variation. E. 2006. Proc. Keck. Kolbe. Oxford. 68A:67–73. 1978. 136:727–741. Near. S. Nystrom. J. 1902. and D. The major features of evolution. 237 pp.. 2003. 144:193–209. 1944. Wainwright. Rabosky. Oxford Univ. T. May. Rapid allopatric speciation in logperch darters (percidae: Percina). N. 1953. Brown. Osborn. O. 2002. W. subgenus Catonotus) with descriptions of two new species. Philipp. Schluter. Evolution 59:1976–1988. Proc. Louis. Nat. M. Near. and D. 2008. A. Lond. Proc. Martins. and H. 1998. Roopnarine. Evolution 59:1768–1782. F. Squamata). Torres-Carvajal. C. 2005. 2006. 2009. M. The law of adaptive radiation. Kassler. Phylogenet. A. M. Lond. M. J. Thum. Theory Methods A7: 13–26.. J. Associate Editor: D. R. B. 2000. 247–265 in J. P. Near. PhD thesis. 172:E270–E284. 1981. and J. Micropterus (Actinopterygii: Centrarchidae). and A. R. and A. St.. 1990. Testing the hypothesis that a clade has adaptively radiated: iguanid lizard clades as a case study. 2005. 6:e71. Bolnick. W. Press. Am. A. Evolution 57:1610–1621. Shochat. It’s about time: the temporal dynamics of phenotypic selection in the wild. Starck and R. McPeek. J. Press. B. J. Losos. J. 2006. S. 2006. 14:3485–3496. 160:147–157. Dillman. ———. K. Supporting Information may be found in the online version of this article. R. and I. 39:171–185. Fossil calibrations and molecular divergence time estimates in centrarchid fishes (teleostei: Centrarchidae). San Francisco. Mooers. Evol. 2001. Variation. Grant. Nee. M. C. Any queries (other than missing material) should be directed to the corresponding author for the article. Mol. E. B. R. Nat. 2002. Molecular phylogenetics and mitochondrial genomic evolution in the Chamaeleonidae (Reptilia. 2005. J. B. and M. Am. B 266:321–329. 296 pp. Mol. T. R. M. Tempo and mode of evolution revealed by molecular phylogenies. D. 1999. Lynch.. Ann. D. B. Posada Supporting Information The following supporting information is available for this article: Appendix includes additional results and analyses. S. Hedges. D. Ruta. Evolution 60:922–933. J. D. and P. B. 2005. Evolution 58:2798–2808. and R. A. Simpson. Polly. H. Ecol. Parallel evolution in ecological and reproductive traits to produce cryptic damselfly species across the Holarctic. Hendry. Comm. H. African cichlid fish: a model system in adaptive radiation research.. Hardman. Koppelman. Press. L. Am. e Testing for different rates of continuous trait evolution using likelihood. J. The ecology of adaptive radiation. Speciation in North American black basses. Further analysis of the data by Akaike’s information criterion and the finite corrections. Mol. B. Wagner. L. 1992. Phylogenetic relationships of South American lizards of the genus Stenocercus (Squamata: Iguania): a new approach using a general mixture model for gene sequence data. B. New York. 165:E78–E107. P. life history and morphology. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. P. ecology. Canada. 2005. Paleontology and the comparative method: ancestral node reconstructions versus observed node values. Nat. Am. Soc. F. Vos. P. and timing of diversification in Nothonotus darters. 12:1261–1276. 2003. Dessauer. Petren. Inferring large phylogenies: the big tree problem. DiBattista. E. Proc. Macroevolution: pattern and process.. and P. Copeia 2003:512–530. D. 36:353–363. Schluter. C. M. Mainland colonization by island lizards. C. M. 2004.. 275:2363–2371. and D.. Lond. Columbia Univ. Oxford. and P. 2396 EVOLUTION AUGUST 2010 . Turgeon. Acad. Am. Ecol. Cadle. I. Density dependent diversification in North American wood-warblers. constraint. R. and S.. Columbia Univ. Glor. 1979. vicariance. Near. 2003.. Vancouver.. J. and M. J. Lovette.. J. PLoS ONE 4:e6876. Townsend. B 273:2107–2111. Density dependent cladogenesis in birds. Simultaneous quaternary radiations of three damselfly clades across the Holarctic. New York.. M. McKellar. J. 1999. Tempo and mode in evolution. Miles. Evol. M. Natl. Stat. A.. Evolutionary patterns in early tetrapods. Soc. Lond. E. P. 23:22–36. M. H A R M O N E T A L . Press. Avian growth and development: evolution within the Altricial-Precocial spectrum. Nat. and M. 370 pp. R. Wainwright. The ecological dynamics of clade diversification and community assembly. M. R. Dispersal. Vamosi. Estimating the rate of phenotypic evolution from comparative data. Schulte. 2008.. and P. R. Near. Sugihara. Simon Fraser Univ. L. Coates. 2009. Seehausen. Losos. 434 pp. H. T. J. Ø. 2008. PLoS Biol. Soc. A phylogeny of Darwin’s finches based on microsatellite DNA length variation. Mooers. B. Nat. E. Pp. S. Phylogenet. 1994. Starck. and T. Pepin. K. O. Larson. Stocks.. J.. Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Grant. D. PhD thesis. Am. A. Page. I. 157:596–609. Nat. McPeek. 2006. Evol. Nicholson. Oxford Univ. B. P. Syst. D. A. McPeek. Analysis of rates of morphological evolution. Biochem. E. Lett. and phylogeny: comparative analysis of variation in growth. C. Nat. An´ . Am. A. 34:605–632. E. and J. USA 89:8322– 8326. Ø.. Comparative immunological study of albumins of Anolis lizards of the Caribbean islands. Washington Univ. G. Mooers.. T. Rev. Phillimore. T. M. R. A. 2001. Harvey. Sci. Am. Using phylogenies to test macroevolutionary hypotheses of trait evolution in cranes (Gruinae). Larson. J. Siepielski. I. Sanderson. M. D. Freeman and Co. CA. Comp. Ecol. A. Stoks. J. Biogeogr. G.. Stanley. Carlson. Natural history of monitor lizards (family Varanidae) with evidence from phylogeny. 154:249–259. and B. Soc. C. B 273:1–12.. R. J. J.L U K E J. A. P. Phylogenetic relationships of barcheek darters (Percidae: Etheostoma. L. O.