Rapid radiations, including adaptive radiations, are of considerable interest to evolutionary biologists, in large part because they are thought to underlie much of the species diversity of life. Yet, this fundamental idea has only been tested at a limited scale, within frogs. Here, we test this idea across living organisms and within many of the largest clades (e.g. animals, plants). Specifically, we quantify how much of Earth’s species richness is contained within rapid radiations (clades with high net diversification rates). We find that among the major clades of living organisms and among land plant phyla and animal phyla, >80% of known species richness is contained within the few clades in the upper 90th percentile for diversification rates in each group. Thus, these exceptionally rapid radiations contain most of Earth’s extant species diversity. Patterns were broadly similar using smaller clades (orders, families) and in insects and vertebrates, with the majority of species generally contained within clades in the upper 75th percentile. Results were also similar using large-scale clades defined by their ages instead of taxonomic ranks. Overall, these results show for the first time that most of the known species richness of life is explained by rapid radiations. Moreover, phenotypic evidence from previous studies suggests that some of the most species-rich rapid radiations across life, animals, and plants may also qualify as adaptive radiations.

Variation of form-function relationships within populations is the substrate for adaptation at higher levels. Therefore, assessing similarity in form-function relationships within and between species may help reveal the processes shaping functional diversity. Here, we test such similarity across three levels of anuran phenotypic divergence: within a population, among species in a single family (Hylidae; ~60 myr), and across a much broader sample of all anuran species using a single microhabitat (arboreal; ~120 myr). We expected less interspecific divergence to show higher similarity of form-function relationships with the intraspecific level. We analyzed the relationships between locomotor performance (in both swimming and jumping) and several hindlimb traits across these three evolutionary levels. While we found a positive correlation between swimming and jumping velocity at both intra- and interspecific levels, relationships between performance and body form did not match across levels. We suggest that different strengths of functional constraints or trade-offs may have produced more variation in form-function relationships across species, decoupling them from within-species patterns. We conclude that performance landscapes are likely qualitatively different across the different evolutionary scales, potentially reflecting changes in the relative importance of different behaviors across all arboreal species.

AbstractUnderstanding whether and why microevolutionary patterns of trait covariation match macroevolutionary divergence is essential for linking evolution at different timescales. However, recent work has focused on developmental constraints for alignment between intraspecific variation and divergence, neglecting a potential role of natural selection on function to connect these scales. Here, we compare the support for the selection and constraint hypotheses to explain both phenotypic trait covariation and species divergence. To test these hypotheses, we collected data on hindlimb and jumping performance traits within and across species of two frog genera. We compared patterns of within-species phenotypic variation (the P matrix) with divergence and selective covariance matrices, from which we could extract the major axes of the realized adaptive landscape (AL), the directions in which adaptive peaks shifted the most over evolutionary time. We also tested whether the major axes of the AL were related to selection on jumping performance. We found high alignment between patterns of variation across scales. Most divergence occurred in allometric size, defined as the first eigenvector of the P matrix. However, jumping performance gradients were unaligned with the major axes of the AL and the P matrix. Across species, however, evolution of maximum acceleration showed a strong negative relationship with changes in allometric size. We infer that the jumping peak evolved under fluctuating selection, and species have tracked the peak along the direction of most within-species variation, allometric size. We conclude that long-term hindlimb divergence was constrained by developmental interactions among traits associated with growth and not net directional selection. Nonetheless, divergence on size indirectly influenced jumping evolution.

Evolution by natural selection and adaptation are core concepts in biology that students must see and correctly understand their meaning. However, using these concepts in evidence-based learning strategies in the classroom is a difficult task. Here, we present a 5E lesson plan to address the Next Generation Science Standards performance expectation HS-LS4-4, to “construct an explanation based on evidence for how natural selection leads to adaptation of populations.” The Functional Frogs lesson provides multiple hands-on activities to engage students in the development of hypotheses, collection and analysis of empirical data on frog swimming, presentation of results, and construction of explanations supported by evidence for the results. The lesson’s central idea is for students to understand the trait values that provide an advantage in the aquatic environment, increasing a frog’s survival. The link between morphological changes and survival is used to explain how natural selection acts on populations, leading to adaptive evolution.

Most of life's vast diversity of species and phenotypes is often attributed to adaptive radiation. Yet its contribution to species and phenotypic diversity of a major group has not been examined. Two key questions remain unresolved. First, what proportion of clades show macroevolutionary dynamics similar to adaptive radiations? Second, what proportion of overall species richness and phenotypic diversity do these adaptive-radiation-like clades contain? We address these questions with phylogenetic and morphological data for 1226 frog species across 43 families (which represent >99% of all species). Less than half of frog families resembled adaptive radiations (with rapid diversification and morphological evolution). Yet, these adaptive-radiation-like clades encompassed ~75% of both morphological and species diversity, despite rapid rates in other clades (e.g., non-adaptive radiations). Overall, we support the importance of adaptive-radiation-like evolution for explaining diversity patterns and provide a framework for characterizing macroevolutionary dynamics and diversity patterns in other groups.

Evolution by natural selection and adaptation are core concepts in biology that students must see and correctly understand their meaning. However, using these concepts in evidence-based learning strategies in the classroom is a difficult task. Here, we present a 5E lesson plan to address the Next Generation Science Standards performance expectation HS-LS4-4, to "construct an explanation based on evidence for how natural selection leads to adaptation of populations." The Functional Frogs lesson provides multiple hands-on activities to engage students in the development of hypotheses, collection and analysis of empirical data on frog swimming, presentation of results, and construction of explanations supported by evidence for the results. The lesson's central idea is for students to understand the trait values that provide an advantage in the aquatic environment, increasing a frog's survival. The link between morphological changes and survival is used to explain how natural selection acts on populations, leading to adaptive evolution.

Abstract Models based on the Ornstein–Uhlenbeck process have become standard for the comparative study of adaptation. Cooper et al. (2016) have cast doubt on this practice by claiming statistical problems with fitting Ornstein–Uhlenbeck models to comparative data. Specifically, they claim that statistical tests of Brownian motion may have too high Type I error rates and that such error rates are exacerbated by measurement error. In this note, we argue that these results have little relevance to the estimation of adaptation with Ornstein–Uhlenbeck models for three reasons. First, we point out that Cooper et al. (2016) did not consider the detection of distinct optima (e.g. for different environments), and therefore did not evaluate the standard test for adaptation. Second, we show that consideration of parameter estimates, and not just statistical significance, will usually lead to correct inferences about evolutionary dynamics. Third, we show that bias due to measurement error can be corrected for by standard methods. We conclude that Cooper et al. (2016) have not identified any statistical problems specific to Ornstein–Uhlenbeck models, and that their cautions against their use in comparative analyses are unfounded and misleading. [adaptation, Ornstein–Uhlenbeck model, phylogenetic comparative method.]

Sexual dimorphism (SD) is a common feature of animals, and selection for sexually dimorphic traits may affect both functional morphological traits and organismal performance. Trait evolution through natural selection can also vary across environments. However, whether the evolution of organismal performance is distinct between the sexes is rarely tested in a phylogenetic comparative context. Anurans commonly exhibit sexual size dimorphism, which may affect jumping performance given the effects of body size on locomotion. They also live in a wide variety of microhabitats. Yet the relationships among dimorphism, performance, and ecology remain underexamined in anurans. Here, we explore relationships between microhabitat use, body size, and jumping performance in males and females to determine the drivers of dimorphic patterns in jumping performance. Using methods for predicting jumping performance through anatomical measurements, we describe how fecundity selection and natural selection associated with body size and microhabitat have likely shaped female jumping performance. We found that the magnitude of sexual size dimorphism (where females are about 14% larger than males) was much lower than dimorphism in muscle volume, where females had 42% more muscle than males (after accounting for body size). Despite these sometimes-large averages, phylogenetic t-tests failed to show the statistical significance of SD for any variable, indicating sexually dimorphic species tend to be closely related. While SD of jumping performance did not vary among microhabitats, we found female jumping velocity and energy differed across microhabitats. Overall, our findings indicate that differences in sex-specific reproductive roles, size, jumping-related morphology, and performance are all important determinants in how selection has led to the incredible ecophenotypic diversity of anurans.

Understanding functional adaptation demands an integrative framework that captures the complex interactions between form, function, ecology, and evolutionary processes. In this review, we discuss how to integrate the following two distinct approaches to better understand functional evolution: (1) the adaptive landscape approach (ALA), aimed at finding adaptive peaks for different ecologies, and (2) the performance landscape approach (PLA), aimed at finding performance peaks for different ecologies. We focus on the Ornstein-Uhlenbeck process as the evolutionary model for the ALA and on biomechanical modeling to estimate performance for the PLA. Whereas both the ALA and the PLA have each given insight into functional adaptation, separately they cannot address how much performance contributes to fitness or whether evolutionary constraints have played a role in form-function evolution. We show that merging these approaches leads to a deeper understanding of these issues. By comparing the locations of performance and adaptive peaks, we can infer how much performance contributes to fitness in species' current environments. By testing for the relevance of history on phenotypic variation, we can infer the influence of past selection and constraints on functional adaptation. We apply this merged framework in a case study of turtle shell evolution and explain how to interpret different possible outcomes. Even though such outcomes can be quite complex, they represent the multifaceted relations among function, fitness, and constraints.

The data available for reconstructing molecular phylogenies have become wildly disparate. Phylogenomic studies can generate data for thousands of genetic markers for dozens of species, but for hundreds of other taxa, data may be available from only a few genes. Can these two types of data be integrated to combine the advantages of both, addressing the relationships of hundreds of species with thousands of genes? Here, we show that this is possible, using data from frogs. We generated a phylogenomic data set for 138 ingroup species and 3,784 nuclear markers (ultraconserved elements [UCEs]), including new UCE data from 70 species. We also assembled a supermatrix data set, including data from 97% of frog genera (441 total), with 1-307 genes per taxon. We then produced a combined phylogenomic-supermatrix data set (a "gigamatrix") containing 441 ingroup taxa and 4,091 markers but with 86% missing data overall. Likelihood analysis of the gigamatrix yielded a generally well-supported tree among families, largely consistent with trees from the phylogenomic data alone. All terminal taxa were placed in the expected families, even though 42.5% of these taxa each had >99.5% missing data and 70.2% had >90% missing data. Our results show that missing data need not be an impediment to successfully combining very large phylogenomic and supermatrix data sets, and they open the door to new studies that simultaneously maximize sampling of genes and taxa.

Comparative phylogenetic studies of adaptation are uncommon in biomechanics and physiology. Such studies require data collection from many species, a challenge when this is experimentally intensive. Moreover, researchers struggle to employ the most biologically appropriate phylogenetic tools for identifying adaptive evolution. Here, we detail an established but greatly underutilized phylogenetic comparative framework - the Ornstein-Uhlenbeck process - that explicitly models long-term adaptation. We discuss challenges in implementing and interpreting the model, and we outline potential solutions. We demonstrate use of the model through studying the evolution of thermal physiology in treefrogs. Frogs of the family Hylidae have twice colonized the temperate zone from the tropics, and such colonization likely involved a fundamental change in physiology due to colder and more seasonal temperatures. However, which traits changed to allow colonization is unclear. We measured cold tolerance and characterized thermal performance curves in jumping for 12 species of treefrogs distributed from the Neotropics to temperate North America. We then conducted phylogenetic comparative analyses to examine how tolerances and performance curves evolved and to test whether that evolution was adaptive. We found that tolerance to low temperatures increased with the transition to the temperate zone. In contrast, jumping well at colder temperatures was unrelated to biogeography and thus did not adapt during dispersal. Overall, our study shows how comparative phylogenetic methods can be leveraged in biomechanics and physiology to test the evolutionary drivers of variation among species.

Miniature insects must overcome significant viscous resistance in order to fly. They typically possess wings with long bristles on the fringes and use a clap-and-fling mechanism to augment lift. These unique solutions to the extreme conditions of flight at tiny sizes (<2 mm body length) suggest that natural selection has optimized wing design for better aerodynamic performance. However, species vary in wingspan, number of bristles (n) and bristle gap (G) to diameter (D) ratio (G/D). How this variation relates to body length (BL) and its effects on aerodynamics remain unknown. We measured forewing images of 38 species of thrips and 21 species of fairyflies. Our phylogenetic comparative analyses showed that n and wingspan scaled positively and similarly with BL across both groups, whereas G/D decreased with BL, with a sharper decline in thrips. We next measured aerodynamic forces and visualized flow on physical models of bristled wings performing clap-and-fling kinematics at a chord-based Reynolds number of 10 using a dynamically scaled robotic platform. We examined the effects of dimensional (G, D, wingspan) and non-dimensional (n, G/D) geometric variables on dimensionless lift and drag. We found that: (1) increasing G reduced drag more than decreasing D; (2) changing n had minimal impact on lift generation; and (3) varying G/D minimally affected aerodynamic forces. These aerodynamic results suggest little pressure to functionally optimize n and G/D. Combined with the scaling relationships between wing variables and BL, much wing variation in tiny flying insects might be best explained by underlying shared growth factors.

The hidden-state speciation and extinction (HiSSE) model helps avoid spurious results when testing whether a character affects diversification rates. However, care must be taken to optimally analyze models and interpret results. Recently, Tonini et al. (TEA hereafter) studied anuran (frog and toad) diversification with HiSSE methods. They concluded that their focal state, breeding in phytotelmata, increases net diversification rates. Yet this conclusion is counterintuitive, because the state that purportedly increases net diversification rates is 14 times rarer among species than the alternative. Herein, I revisit TEA's analyses and demonstrate problems with inferring model likelihoods, conducting post hoc tests, and interpreting results. I also reevaluate their top models and find that diverse strategies are necessary to reach the parameter values that maximize each model's likelihood. In contrast to TEA, I find no support for an effect of phytotelm breeding on net diversification rates in Neotropical anurans. In particular, even though the most highly supported models include the focal character, averaging parameter estimates over hidden states shows that the focal character does not influence diversification rates. Finally, I suggest ways to better analyze and interpret complex diversification models-both state-dependent and beyond-for future studies in other organisms.

Summary The functioning of present ecosystems reflects deep evolutionary history of locally cooccurring species if their functional traits show high phylogenetic signal (PS). However, we do not understand what drives local PS. We hypothesize that local PS is high in undisturbed and stressful habitats, either due to ongoing local assembly of species that maintained ancestral traits, or to past evolutionary maintenance of ancestral traits within habitat species‐pools, or to both. We quantified PS and diversity of 10 traits within 6704 local plant communities across 38 Dutch habitat types differing in disturbance or stress. Mean local PS varied 50‐fold among habitat types, often independently of phylogenetic or trait diversity. Mean local PS decreased with disturbance but showed no consistent relationship to stress. Mean local PS exceeded species‐pool PS, reflecting nonrandom subsampling from the pool. Disturbance or stress related more strongly to mean local than to species‐pool PS. Disturbed habitats harbour species with evolutionary divergent trait values, probably driven by ongoing, local assembly of species: environmental fluctuations might maintain different trait values within lineages through an evolutionary storage effect. If functional traits do not reflect phylogeny, ecosystem functioning might not be contingent on the presence of particular lineages, and lineages might establish evolutionarily novel interactions.

Appendix S1 (“AppendixS1_all_bristle_data.csv”; “AppendixS1_all_bristle_data.xlsx”): All phenotypic data used in the analyses of thrips and fairyfly wings. The CSV file is for replicating analyses in R. The MS Excel file includes a metadata tab that explains the variables and units.Appendix S2 (“AppendixS2_bristled_wings_tree_simulation.R”): R code for replicating the phylogeny simulations for downstream phylogenetic comparative analyses.Appendix S3 (“AppendixS3_all_family_list.csv”): A taxonomy of thrips and fairyfly genera. The file is used in Appendix S2 for simulating phylogenies. Taxonomic sources are listed in the methods of the published paper.Appendix S4 (“AppendixS4_10000random_trees.tre”): The 10,000 simulated phylogenies used for phylogenetic comparative analyses in this paper.Appendix S5 (“AppendixS5_bristled_wings_PCMs.R”): R code for replicating all phylogenetic regression and correlation analyses in the paper. This also includes code for replicating figures of phenotypic data.Appendix S6 (“AppendixS6_bristled_wings_fxns.R”): Auxiliary functions used in Appendix S5. This file is called directly in Appendix S5 (i.e. no need to manually load the functions).

Adaptive radiation is a key topic at the intersection of ecology and evolutionary biology. Yet the definition and identification of adaptive radiation both remain contentious. Here, we introduce a new approach for identifying adaptive radiations that combines key aspects of two widely used definitions. Our approach compares evolutionary rates in morphology, performance, and diversification between the candidate radiation and other clades. We then apply this approach to a putative adaptive radiation of frogs from Madagascar (Mantellidae). We present new data on morphology and performance from mantellid frogs, then compare rates of diversification and multivariate evolution of size, shape, and performance between mantellids and other frogs. We find that mantellids potentially pass our test for accelerated rates of evolution for shape, but not for size, performance, or diversification. Our results demonstrate that clades can have accelerated phenotypic evolution without rapid diversification (dubbed "adaptive non-radiation"). We also highlight general issues in testing for adaptive radiation, including taxon sampling and the problem of including another adaptive radiation among the comparison clades. Finally, we suggest that similar tests should be conducted on other putative adaptive radiations on Madagascar, comparing their evolutionary rates to those of related clades outside Madagascar. Based on our results, we speculate that older Madagascar clades may show evolutionary patterns more similar to those on a continent than an island.

Anuran (frog and toad) jumping power varies greatly across species, yet muscle power does not. Given that the jumping power of some species is up to five times higher than typical muscle power, power amplification by elastic elements is suggested to explain this discrepancy. However, the ecological reasons for this variation in jumping power remain unclear. One hypothesis is that small jumpers are limited by the time available to accelerate their body during take-off, leading to small species needing greater power production than larger species to achieve similar jumping performance. Another (non-mutually exclusive) hypothesis is that the microhabitat species inhabit may drive variation through trade-offs with performance in microhabitat-specific, non-jumping behaviours. We compared jumping power across 68 anuran species that were diverse in evolutionary relationships, microhabitat use and body mass. We used phylogenetic comparative methods to compare the role of microhabitat and body mass in explaining variation in jumping power across species. We found the strongest support for a model that included two factors and their interaction. First, as body mass increased, jumping power decreased. Second, species that burrowed showed lower jumping power than species that did not burrow. Third, the interaction between body mass and burrowing behaviour showed that jumping power declines more rapidly with body mass in burrowing species than non-burrowing species. The effect of body mass suggests that interspecific variation in jumping power might be partly explained by scaling relationships. Anurans with small body mass may be able to achieve similar locomotor performance (e.g. takeoff velocity) as those with larger body mass, by more effectively amplifying muscle power. Additionally, the effect of burrowing behaviour suggests that species that use hindlimbs to burrow may experience a reduction in their ability to generate jumping power. This may indicate a functional trade-off between jumping and burrowing performance. A free Plain Language Summary can be found within the Supporting Information of this article.

Organismal performance is often key in understanding macroevolutionary patterns but characterizing performance across many species is challenging, as the disparate geographic locations of taxa often prohibit in vivo measures. In theory, however, inferences on the evolution of performance could be investigated using anatomical approximations of performance parameters, allowing for a wider range of species to be sampled. In this study, we use biological and physical principles to mathematically derive three size-standardized anatomical approximations for three different aspects of jumping performance at take-off in anurans: peak jumping velocity, energy, and power. We also describe several ways to parameterize these approximations using, for example, measurements of leg length, leg muscle mass, and body mass. We evaluate the efficacy of these approaches via comparison with direct size-standardized measures of jumping performance across 256 individuals from 51 anuran species. Using both phylogenetic and non-phylogenetic approaches, we find that two of the three anatomical approximations (velocity and energy) are highly correlated with in vivo measures, while a third (power) is not. This reveals that the former may serve as reliable estimates of those aspects of jumping performance, while the latter approximation does not capture all aspects of jumping power in anurans. We also report significant phylogenetic signal for the approximations, as found in in vivo measures. These analyses demonstrate the utility of anatomical approximations for use in macroevolutionary studies. Relative to in vivo laboratory methods, this new method allows for broad museum-based taxonomic surveys of jumping performance in anurans and possibly other jumping animals.

Organisms inhabiting a specific environment often have distinct morphology, but the factors that affect this fit are unclear when multiple morphological traits affect performance in multiple behaviors. Does the realized morphology of a species reflect a compromise in performance among behaviors (i.e., trade-offs)? Or does many-to-one mapping result in morphological distinctness without compromising performance across behaviors? The importance of these principles in organismal design has rarely been compared at the macroevolutionary scale. Here I study 191 species of frogs from around the world that inhabit different microhabitats, using models of phenotypic evolution to examine how form-function relationships may explain the fit between ecology and morphology. I found three key results. First, despite being distinct in leg morphology, ecomorphs were similar in jumping performance. Second, ecomorphs that regularly swim showed higher swimming performance, which paralleled the higher leg muscle mass in these taxa. Third, many-to-one mapping of form onto function occurred at all but the highest levels of both jumping and swimming performance. The seemingly contradictory first two results were explained by the third: when one behavior occurs in all species while another is restricted to a subset, many-to-one mapping allows species with distinct ecologies to have distinct body forms that reflect their specialized behavior while maintaining similar performance in a more general shared behavior.

Geckos are a highly diverse group of lizards, with more than 1,700 species that exhibit a wide range of behaviors, ecologies, and sizes. However, no study has examined links between habitat use and body shape in pad-bearing geckos. We set out to answer a basic question using a data set of pad-bearing geckos (112 species, 103 pad-bearing, 9 padless, 42 genera): Do geckos that occur in different habitats also differ in body shape? Overall, we found that body shape was surprisingly similar among our sample of pad-bearing species, with the exception of the genus Uroplatus, which was clearly distinct from other geckos due to its depressed body and long limbs. However, the padless geckos differed in body shape from the pad-bearing geckos by having longer arms and legs and less rotund bodies. We found that about half of the pad-bearing species primarily inhabit trees, with the other half, divided approximately equally among rocks, the ground, and mixed habitats. We found no significant links between habitat use and body shape, nor any propensity for larger species to occupy different habitats than smaller species. Padless species tend to inhabit rock and ground substrates. Our results indicate that pad-bearing geckos have a relatively uniform body form, which contrasts with to their diversity in color, size, and behavior. Indeed, our data show that the general gecko body shape is suitable for a wide range of habitats, ranging from arboreal to terrestrial. This pattern is a departure from other ecomorphological studies and suggests that geckos may not easily fit into the mold of adaptive radiation, as suggested by prior studies.