When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.     

Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification

Competition can drive macroevolutionary change, for example during adaptive radiations. However, we still lack a clear understanding of how it shapes diversification processes and patterns. To better understand the macroevolutionary consequences of competition, as well as the signal left on phylogenetic data, we developed a model linking trait evolution and species diversification in an ecological context. We find four main results: first, competition spurs trait diversity but not necessarily species richness; second, competition produces slowdowns in species diversification even in the absence of explicit ecological limits, but not in phenotypic diversification even in the presence of such limits; third, early burst patterns do not provide a reliable way of testing for adaptive radiations; and fourth, looking for phylogenetic signal in trait data and support for phenotypic models incorporating competition is a better alternative. Our results clarify the macroevolutionary consequences of competition and could help design more powerful tests of adaptive radiations in nature.     

Hierarchy in adaptive radiation: A case study using the Carnivora (Mammalia)

Simpson's “early burst” model of adaptive radiation was intended to explain the early proliferation of morphological and functional variation in diversifying clades. Yet, despite much empirical testing, questions remain regarding its frequency across the tree of life. Here, we evaluate the support for an early burst model of adaptive radiation in 14 ecomorphological traits plus body mass for the extant mammalian order Carnivora and its constituent families. We find strong support for early bursts of dental evolution, suggesting a classic Simpsonian adaptive radiation along dietary resource axes. However, the signal of this early burst is not consistently recovered in analyses at the family level, where support for a variety of different models emerges. Furthermore, we find no evidence for early burst–like dynamics in size–related traits, and Bayesian analyses of evolutionary correlations corroborate a decoupling of size and dental evolution, driven in part by dietary specialization. Our results are consistent with the perspective that trait diversification unfolds hierarchically, with early bursts restricted to traits associated with higher level niches, such as macrohabitat use or dietary strategy, and thus with the origins of higher taxa. The lack of support for early burst adaptive radiation in previous phylogenetic studies may be a consequence of focusing on low‐level niche traits (i.e., those associated with microhabitat use) in clades at shallow phylogenetic levels. A richer understanding of early burst adaptive radiation will require a renewed focus on functional traits and their evolution over higher level clades.     

Correlated evolution between climate and suites of traits along a fast–slow continuum in the radiation of Protea

Evolutionary radiations are responsible for much of Earth's diversity, yet the causes of these radiations are often elusive. Determining the relative roles of adaptation and geographic isolation in diversification is vital to understanding the causes of any radiation, and whether a radiation may be labeled as “adaptive” or not. Across many groups of plants, trait–climate relationships suggest that traits are an important indicator of how plants adapt to different climates. In particular, analyses of plant functional traits in global databases suggest that there is an “economics spectrum” along which combinations of functional traits covary along a fast–slow continuum. We examine evolutionary associations among traits and between trait and climate variables on a strongly supported phylogeny in the iconic plant genus Protea to identify correlated evolution of functional traits and the climatic‐niches that species occupy. Results indicate that trait diversification in Protea has climate associations along two axes of variation: correlated evolution of plant size with temperature and leaf investment with rainfall. Evidence suggests that traits and climatic‐niches evolve in similar ways, although some of these associations are inconsistent with global patterns on a broader phylogenetic scale. When combined with previous experimental work suggesting that trait–climate associations are adaptive in Protea, the results presented here suggest that trait diversification in this radiation is adaptive.     

Diversity versus disparity and the radiation of modern cetaceans

Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.     

Parallel adaptations to nectarivory in parrots,key innovations and the diversification of the Loriinae

Specialization to nectarivory is associated with radiations within different bird groups, including parrots. One of them, the Australasian lories, were shown to be unexpectedly species rich. Their shift to nectarivory may have created an ecological opportunity promoting species proliferation. Several morphological specializations of the feeding tract to nectarivory have been described for parrots. However, they have never been assessed in a quantitative framework considering phylogenetic nonindependence. Using a phylogenetic comparative approach with broad taxon sampling and 15 continuous characters of the digestive tract, we demonstrate that nectarivorous parrots differ in several traits from the remaining parrots. These trait‐changes indicate phenotype–environment correlations and parallel evolution, and may reflect adaptations to feed effectively on nectar. Moreover, the diet shift was associated with significant trait shifts at the base of the radiation of the lories, as shown by an alternative statistical approach. Their diet shift might be considered as an evolutionary key innovation which promoted significant non‐adaptive lineage diversification through allopatric partitioning of the same new niche. The lack of increased rates of cladogenesis in other nectarivorous parrots indicates that evolutionary innovations need not be associated one‐to‐one with diversification events.     

Ecomorphological disparity in an adaptive radiation: opercular bone shape and stable isotopes in Antarctic icefishes

To assess how ecological and morphological disparity is interrelated in the adaptive radiation of Antarctic notothenioid fish we used patterns of opercle bone evolution as a model to quantify shape disparity, phylogenetic patterns of shape evolution, and ecological correlates in the form of stable isotope values. Using a sample of 25 species including representatives from four major notothenioid clades, we show that opercle shape disparity is higher in the modern fauna than would be expected under the neutral evolution Brownian motion model. Phylogenetic comparative methods indicate that opercle shape data best fit a model of directional selection (Ornstein–Uhlenbeck) and are least supported by the “early burst” model of adaptive radiation. The main evolutionary axis of opercle shape change reflects movement from a broad and more symmetrically tapered opercle to one that narrows along the distal margin, but with only slight shape change on the proximal margin. We find a trend in opercle shape change along the benthic–pelagic axis, underlining the importance of this axis for diversification in the notothenioid radiation. A major impetus for the study of adaptive radiations is to uncover generalized patterns among different groups, and the evolutionary patterns in opercle shape among notothenioids are similar to those found among other adaptive radiations (three‐spined sticklebacks) promoting the utility of this approach for assessing ecomorphological interactions on a broad scale.     

The ecology of a continental evolutionary radiation: Is the radiation of sigmodontine rodents adaptive?

Evolutionary radiations on continents are less well‐understood and appreciated than those occurring on islands. The extent of ecological influence on species divergence can be evaluated to determine whether a radiation was ultimately the outcome of divergent natural selection or else arose mainly by nonecological divergence. Here, we used phylogenetic comparative methods to test distinct hypotheses corresponding to adaptive and nonadaptive evolutionary scenarios for the morphological evolution of sigmodontine rodents. Results showed that ecological variables (diet and life‐mode) explain little of the shape and size variation of sigmodontine skulls and mandibles. A Brownian model with varying rates for insectivory versus all other diets was the most likely evolutionary model. The insectivorous sigmodontines have a faster rate of morphological evolution than mice feeding on other diets, possibly due to stronger selection for features that aid insectivory. We also demonstrate that rapid early‐lineage diversification is not accompanied by high morphological divergence among subclades, contrasting with island results. The geographic size of continents permits spatial segregation to a greater extent than on islands, allowing for allopatric distributions and escape from interspecific competition. We suggest that continental radiations of rodents are likely to produce a pattern of high species diversification coupled with a low degree of phenotypic specialization.     

How traits shape trees: new approaches for detecting character state‐dependent lineage diversification

Biologists have long sought to understand the processes underlying disparities in clade size across the tree of life and the extent to which such clade size differences can be attributed to the evolution of particular traits. The association of certain character states with species‐rich clades suggests that trait evolution can lead to increased diversification, but such a pattern could also arise due other processes, such as directional trait evolution. Recent advances in phylogenetic comparative methods have provided new statistical approaches for distinguishing between these intertwined and potentially confounded macroevolutionary processes. Here, we review the historical development of methods for detecting state‐dependent diversification and explore what new methods have revealed about classic examples of traits that affect diversification, including evolutionary dead ends, key innovations and geographic traits. Applications of these methods thus far collectively suggest that trait diversity commonly arises through the complex interplay between transition, speciation and extinction rates and that long hypothesized evolutionary dead ends and key innovations are instead often cases of directional trends in trait evolution.     

When are adaptive radiations replicated in areas? Ecological opportunity and unexceptional diversification in West Indian dipsadine snakes (Colubridae: Alsophiini)

Aim We examine diversification in Caribbean alsophiine snakes and hypothesize that, given the ecological opportunity presented by colonization of the West Indies, alsophiines should show the signature of an early burst of diversification and associated low within‐clade ecological and morphological disparification. We also test whether changes in morphology and ecology are associated with changes in diversification rate, as trait‐dependent diversification is hypothesized to affect historical inferences of diversification and disparification. Finally, as replicated radiations are found across the West Indies in the anoles, we test for significant differences in ecological and morphological assemblages and rates among the major island groups. Location The West Indies. Methods A time‐calibrated phylogeny produced from six genes using relaxed clock methods in beast was constructed to estimate ancestral areas using Lagrange . Maximum body size and ecological niche were scored for all species in the phylogeny, and comparative phylogenetic methods in R using geiger , laser , ape and our own code were used to examine diversification through time, disparification and trait‐dependent diversification from this dated phylogeny. Results The pattern of species diversification did not differ significantly from the Yule model of diversification. Morphology and ecology fitted a Brownian and white noise model of diversification, respectively. Although not significantly different, morphological disparification was lower than the Brownian null model, whereas ecological disparification was significantly greater than the null. Trait‐dependent diversification analyses suggested that the constant null models provided the best fit to these data. There was no significant signal of rate variation among the major island groups for size, but moderate evidence for niche. Main conclusions Although ecological opportunity was similarly present for alsophiines as it was for anoles, the snakes fail to show an early burst of speciation. Potential reasons for this include the young age of the group, and staggered diversification due to waiting times between island colonization. In turn, ecological and morphological disparities do not necessarily follow predictable patterns related to species diversification. Thus, the presence of ecological opportunity alone is not necessarily sufficient to trigger replicated adaptive radiations in areas.     

Detecting non-Brownian trait evolution in adaptive radiations

Many phylogenetic comparative methods that are currently widely used in the scientific literature assume a Brownian motion model for trait evolution, but the suitability of that model is rarely tested, and a number of important factors might affect whether this model is appropriate or not. For instance, we might expect evolutionary change in adaptive radiations to be driven by the availability of ecological niches. Such evolution has been shown to produce patterns of change that are different from those modelled by the Brownian process. We applied two tests for the assumption of Brownian motion that generally have high power to reject data generated under non-Brownian niche-filling models for the evolution of traits in adaptive radiations. As a case study, we used these tests to explore the evolution of feeding adaptations in two radiations of warblers. In one case, the patterns revealed do not accord with Brownian motion but show characteristics expected under certain niche-filling models.     

Trait-dependent diversification and the impact of palaeontological data on evolutionary hypothesis testing in New World ratsnakes (tribe Lampropeltini)

For studies investigating trait evolution, there are at least two important questions. First, have traits under consideration influenced cladogenesis and extinction in the group? Second, how do fossil data alter inferences about trait evolution or diversification‐rate dynamics? However, relatively few studies have assessed these questions. Here, we use recently developed methods to test for trait‐dependent diversification in the New World colubrid snake tribe Lampropeltini. We also integrate data from fossil taxa into phylogenetic estimation of evolutionary parameters using a simple Monte Carlo randomization test. These analyses suggest that ecological conditions in temperate regions are tied to higher rates of cladogenesis, but that body size is not related to diversification in the group. We also find that the inclusion of fossil taxa alters absolute estimates of size and the rate of size evolution, but not the overall pattern of ecomorphological diversification, as well as estimates of evolutionary rates, particularly extinction.     

Enemy at the gates: Rapid defensive trait diversification in an adaptive radiation of lizards

Adaptive radiation (AR), the product of rapid diversification of an ancestral species into novel adaptive zones, has become pivotal in our understanding of biodiversity. Although it has widely been accepted that predators may drive the process of AR by creating ecological opportunity (e.g., enemy‐free space), the role of predators as selective agents in defensive trait diversification remains controversial. Using phylogenetic comparative methods, we provide evidence for an “early burst” in the diversification of antipredator phenotypes in Cordylinae, a relatively small AR of morphologically diverse southern African lizards. The evolution of body armor appears to have been initially rapid, but slowed down over time, consistent with the ecological niche‐filling model. We suggest that the observed “early burst” pattern could be attributed to shifts in vulnerability to different types of predators (i.e., aerial versus terrestrial) associated with thermal habitat partitioning. These results provide empirical evidence supporting the hypothesis that predators or the interaction therewith might be key components of ecological opportunity, although the way in which predators influence morphological diversification requires further study.     

Phylogeographic and phenotypic outcomes of brown anole colonization across the Caribbean provide insight into the beginning stages of an adaptive radiation

Some of the most important insights into the ecological and evolutionary processes of diversification and speciation have come from studies of island adaptive radiations, yet relatively little research has examined how these radiations initiate. We suggest that Anolis sagrei is a candidate for understanding the origins of the Caribbean Anolis adaptive radiation and how a colonizing anole species begins to undergo allopatric diversification, phenotypic divergence and, potentially, speciation. We undertook a genomic and morphological analysis of representative populations across the entire native range of A. sagrei, finding that the species originated in the early Pliocene, with the deepest divergence occurring between western and eastern Cuba. Lineages from these two regions subsequently colonized the northern Caribbean. We find that at the broadest scale, populations colonizing areas with fewer closely related competitors tend to evolve larger body size and more lamellae on their toepads. This trend follows expectations for post‐colonization divergence from progenitors and convergence in allopatry, whereby populations freed from competition with close relatives evolve towards common morphological and ecological optima. Taken together, our results show a complex history of ancient and recent Cuban diaspora with populations on competitor‐poor islands evolving away from their ancestral Cuban populations regardless of their phylogenetic relationships, thus providing insight into the original diversification of colonist anoles at the beginning of the radiation. Our research also supplies an evolutionary framework for the many studies of this increasingly important species in ecological and evolutionary research.     

The role of ecological opportunity in shaping disparate diversification trajectories in a bicontinental primate radiation

Exceptional species and phenotypic diversity commonly are attributed to ecological opportunity (EO). The conventional EO model predicts that rates of lineage diversification and phenotypic evolution are elevated early in a radiation only to decline later in response to niche availability. Foregut fermentation is hypothesized to be a key innovation that allowed colobine monkeys (subfamily Colobinae), the only primates with this trait, to successfully colonize folivore adaptive zones unavailable to other herbivorous species. Therefore, diversification rates also are expected to be strongly linked with the evolution of traits related to folivory in these monkeys. Using dated molecular phylogenies and a dataset of feeding morphology, I test predictions of the EO model to evaluate the role of EO conferred by foregut fermentation in shaping the African and Asian colobine radiations. Findings from diversification methods coupled with colobine biogeographic history provide compelling evidence that decreasing availability of new adaptive zones during colonization of Asia together with constraints presented by dietary specialization underlie temporal changes in diversification in the Asian but not African clade. Additionally, departures from the EO model likely reflect iterative diversification events in Asia.     

Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification

Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan‐tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time‐dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time‐dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs.     

Strong conservatism of floral morphology during the rapid diversification of the genus Helianthemum

Premise

Divergence of floral morphology and breeding systems are often expected to be linked to angiosperm diversification and environmental niche divergence. However, available evidence for such relationships is not generalizable due to different taxonomic, geographical and time scales. The Palearctic genus Helianthemum shows the highest diversity of the family Cistaceae in terms of breeding systems, floral traits, and environmental conditions as a result of three recent evolutionary radiations since the Late Miocene. Here, we investigated the tempo and mode of evolution of floral morphology in the genus and its link with species diversification and environmental niche divergence.

Methods

We quantified 18 floral traits from 83 taxa and applied phylogenetic comparative methods using a robust phylogenetic framework based on genotyping-by-sequencing data.

Results

We found three different floral morphologies, putatively related to three different breeding systems: type I, characterized by small flowers without herkogamy and low pollen to ovule ratio; type II, represented by large flowers with approach herkogamy and intermediate pollen to ovule ratio; and type III, featured by small flowers with reverse herkogamy and the highest pollen to ovule ratio. Each morphology has been highly conserved across each radiation and has evolved independently of species diversification and ecological niche divergence.

Conclusions

The combined results of trait, niche, and species diversification ultimately recovered a pattern of potentially non-adaptive radiations in Helianthemum and highlight the idea that evolutionary radiations can be decoupled from floral morphology evolution even in lineages that diversified in heterogeneous environments as the Mediterranean Basin.     

Ecological opportunity and ecomorphological convergence in Australasian robins (Petroicidae)

Ecological theories of adaptive radiation predict that ecological opportunity (EO) stimulates cladogenesis through entry into a novel environment and/or release of competition pressures. Due to its dynamic paleoclimatic and geological history, the Australo‐Papuan region constitutes an opportune scenario to study patterns of diversification in relation to the colonization of new ecological niches. Here, we employ a comparative framework using the Australasian robins (Petroicidae) as a model system to test whether the diversification of this bird family fulfils a niche‐filling process as predicted by the EO model, and to test whether the observed morphological similarity is described by a pattern of phylogenetic niche conservatism (PNC) or convergence. Although we detected an early‐burst, we did not find a slowdown in speciation or morphological evolution as expected in a niche‐filling scenario. Divergence in tarsus length and tail length (PC1) was consistent with a multi‐peak model, in which PC1 represents a convergent trait among distantly related clades sharing the same foraging strategy. Our study thus shows that convergence rather than PNC seems to explain the existence of morphological similarity across independent lineages in the Petroicidae. We also found a low level of PNC regarding annual variations in temperature and precipitation, which is in agreement with the hypothesis that diversification within the Petroicidae involved repeated radiations. We suggest two non‐mutually exclusive hypotheses to explain the overall lack of density‐dependent cladogenesis. First, the extreme spatial and temporal heterogeneity of this region may have generated a pattern of repeated ecological opportunity over time and, second, this family may not yet have reached equilibrium diversity.     

Early burst in body size evolution is uncoupled from species diversification in diving beetles (Dytiscidae)

Changes in morphology are often thought to be linked to changes in species diversification, which is expected to leave a signal of early burst (EB) in phenotypic traits. However, such signal is rarely recovered in empirical phylogenies, even for groups with well‐known adaptive radiation. Using a comprehensive phylogenetic approach in Dytiscidae, which harbours ~4,300 species with as much as 50‐fold variation in body size among them, we ask whether pattern of species diversification correlates with morphological evolution. Additionally, we test whether the large variation in body size is linked to habitat preference and whether the latter influences species turnover. We found, in sharp contrast to most animal groups, that Dytiscidae body size evolution follows an early‐burst model with subsequent high phylogenetic conservatism. However, we found no evidence for associated shifts in species diversification, which point to an uncoupled evolution of morphology and species diversification. We recovered the ancestral habitat of Dytiscidae as lentic (standing water), with many transitions to lotic habitat (running water) that are concomitant to a decrease in body size. Finally, we found no evidence for difference in net diversification rates between habitats nor difference in turnover in lentic and lotic species. This result, together with recent findings in dragonflies, contrasts with some theoretical expectations of the habitat stability hypothesis. Thus, a thorough reassessment of the impact of dispersal, gene flow and range size on the speciation process is needed to fully encompass the evolutionary consequences of the lentic–lotic divide for freshwater fauna.     

Diversity and disparity through time in the adaptive radiation of Antarctic notothenioid fishes

According to theory, adaptive radiation is triggered by ecological opportunity that can arise through the colonization of new habitats, the extinction of antagonists or the origin of key innovations. In the course of an adaptive radiation, diversification and morphological evolution are expected to slow down after an initial phase of rapid adaptation to vacant ecological niches, followed by speciation. Such ‘early bursts’ of diversification are thought to occur because niche space becomes increasingly filled over time. The diversification of Antarctic notothenioid fishes into over 120 species has become one of the prime examples of adaptive radiation in the marine realm and has likely been triggered by an evolutionary key innovation in the form of the emergence of antifreeze glycoproteins. Here, we test, using a novel time‐calibrated phylogeny of 49 species and five traits that characterize notothenioid body size and shape as well as buoyancy adaptations and habitat preferences, whether the notothenioid adaptive radiation is compatible with an early burst scenario. Extensive Bayesian model comparison shows that phylogenetic age estimates are highly dependent on model choice and that models with unlinked gene trees are generally better supported and result in younger age estimates. We find strong evidence for elevated diversification rates in Antarctic notothenioids compared to outgroups, yet no sign of rate heterogeneity in the course of the radiation, except that the notothenioid family Artedidraconidae appears to show secondarily elevated diversification rates. We further observe an early burst in trophic morphology, suggesting that the notothenioid radiation proceeds in stages similar to other prominent examples of adaptive radiation.