Early Burst Model Research Articles

Investigating the evolutionary dynamics of diploid number variation in Ctenomys (Ctenomyidae, Rodentia).

Contrary to predictions from classical hybrid sterility models of chromosomal speciation, some organisms display high rates of karyotype variation. Ctenomys are the current mammals with the greatest interspecific and intraspecific chromosomal variation. A large number of species have been studied cytogenetically. The diploid numbers of chromosomes range from 2n = 10 to 2n = 70. Here, we analyzed karyotype evolution in Ctenomys using comparative phylogenetic methods. We found a strong phylogenetic signal with chromosome number. This refutes the chromosomal megaevolution model, which proposes the independent accumulation of multiple chromosomal rearrangements in each closely related species. We found that Brownian motion (BM) described the observed characteristic changes more thoroughly than the Ornstein-Uhlenbeck and Early-Burst models. This suggests that the evolution of chromosome numbers occurs by a random walk along phylogenetic clades. However, our data indicate that the BM model alone does not fully characterize the chromosomal evolution of Ctenomys.

On the covariance of phylogenetic quantitative trait evolution models and their matrix condition

Phylogenetic comparative methods (PCMs) use phylogenetic tree and trait data to explore the evolutionary information among a group of related species. Given a phylogenetic tree of extant species, the evolutionary evidence among a group of species can be represented by a squared matrix C obtained by an isomorphic transformation using the shared branch lengths in the tree. The quantitative trait evolution for species along the branch can be described by stochastic processes. Currently, most statistical models for trait evolution are built under the assumption of Gaussian processes, where the trait vector Y follows a multivariate normal distribution with covariance matrix V , transformed from the C matrix and model parameters. This study investigates the effects on parameter estimation in phylogenetic comparative methods that are caused by ill-conditioned phylogenetic tree matrices ( C matrix) and their associated model-adjusted variance–covariance matrices ( V matrix). Several popular models—the Brownian motion model, the Ornstein–Uhlenbeck model, the early burst model, and the phylogenetic mixed model (Pagel’s λ)—are evaluated and compared through an empirical dataset and extensive simulations. Suggestions are provided to users in the community for identifying and overcoming potential issues with their own data.

Phylogenetic patterns of trait and trait plasticity evolution: Insights from tadpoles.

Environmental heterogeneity has led to the widespread evolution of phenotypic plasticity in all taxonomic groups. Although phenotypic plasticity has been examined from multiple perspectives, few studies have examined evolutionary patterns of plasticity within a phylogeny. We conducted common-garden experiments on 20 species of tadpoles, spanning three families, exposed for 4 weeks to a control, predator cues, or reduced food (i.e., increased intraspecific competition). We quantified tadpole activity, growth, and relative morphology and found widespread differences in species responses to predator cues and reduced food. We detected pervasive phylogenetic signals in traits within each environment, but the phylogenetic signal was much less common in the trait plasticities. Among different models of continuous character evolution, Brownian Motion and Ornstein Uhlenbeck models provided better fits to the data than the Early Burst model. Tadpole activity level in predator environments had much higher evolutionary rates than in the control and reduced-food environments; we did not see this pattern in the other traits. In comparing traits versus trait plasticities, activity evolved much faster than the plasticity of activity whereas morphological traits evolved much slower than morphological plasticities. Collectively, these results suggest that traits and trait plasticities can exhibit dramatically different evolutionary patterns.

The non-gradual nature of adaptive radiation

Adaptive radiation is a major source of biodiversity. Still, many aspects of this evolutionary process remain poorly understood. Our recent integrative examination of the cichlid adaptive radiation in African Lake Tanganyika provides new insights into the process of explosive diversification. The in-depth phylogenetic comparative analysis of nearly all species occurring in that lake permitted us to trace patterns of eco-morphological evolution throughout the phylogenetic history of the radiation and revealed that it occurred in a non-gradual manner, in the form of time-shifted bursts of accelerated evolution. The temporal pattern of divergence along different axes of morphological evolution provides empirical support for a scenario that potentially unifies two popular models of adaptive radiation, the “early burst model” and the “stages model”.

The Elevation does not strongly influence interspecific variation in body size of small Tropical endotherms

Introduction: Body size is an essential trait for endotherms to face the physiological requirements of cold, so there is a tendency to large body size at high altitudes and latitudes, known as Bergmann's rule. However, the validity of this ecomorphological rule to small-bodied endotherms across altitudinal gradients is poorly known. Objective: To understand the effects of environmental variation on body size, we assessed whether interspecific variation in body size of small tropical endotherms follows Bergmann's rule along tropical altitudinal gradients. Methods: We compiled data on elevational ranges and body masses for 133 species of hummingbirds of Colombia. We then assessed the association between body mass and mid-point of the altitudinal distribution using phylogenetic generalized least squares (PGLS) analyses under different evolutionary models. Results: We found a decelerating rate of evolution for body size since the Early Burst model of evolution provided a better fit to body mass data. For elevational range, we found a slow and constant rate since Pagel's lambda model provided a better fit to the mid-point of the altitudinal distribution data. Besides, phylogenetic regression analysis indicated that body mass and the altitudinal range of hummingbirds are associated through the phylogeny, with a positive but slight association (R2= 0.036). Conclusions: We found that body mass and altitude of hummingbirds are positively related, which is in agreement with expectations under Bergmann's rule. However, this association was weaker than expected for small and non-passerine birds like hummingbirds. Thus, our results suggest that environmental changes across altitudinal gradients do not strongly influence body mass in small tropical endotherms as hummingbirds.

Paleozoic ammonoid ecomorphometrics test ecospace availability as a driver of morphological diversification.

The early burst model suggests that disparity rises rapidly to fill empty ecospace following clade origination or in the aftermath of a mass extinction. Early bursts are considered common features of fossil data, but neontological studies have struggled to identify them. Furthermore, tests have proven difficult because factors besides ecology can drive changes in morphology. Here, we document the ecomorphometric evolution of the extinct Ammonoidea at 1-million-year resolution, from their origination in the Early Devonian (Emsian) to the Early Triassic (Induan), over ~156 million years. This time interval encompasses six global extinction events, including two of the Big Five, and incorporates multiple ammonoid radiations. However, we find no evidence for early bursts of ecomorphological disparity. This contradicts arguments that the temporal scope, or traits measured in genomic data, conceal evidence of early bursts. Rather, early bursts may be less prevalent in fossil data than is often assumed.

The complex effects of mass extinctions on morphological disparity.

Studies of biodiversity through deep time have been a staple for biologists and paleontologists for over 60 years. Investigations of species richness (diversity) revealed that at least five mass extinctions punctuated the last half billion years, each seeing the rapid demise of a large proportion of contemporary taxa. In contrast to diversity, the response of morphological diversity (disparity) to mass extinctions is unclear. Generally, diversity and disparity are decoupled, such that diversity may decline as morphological disparity increases, and vice versa. Here, we develop simulations to model disparity changes across mass extinctions using continuous traits and birth-death trees. We find no simple null for disparity change following a mass extinction but do observe general patterns. The range of trait values decreases following either random or trait-selective mass extinctions, whereas variance and the density of morphospace occupation only decline following trait-selective events. General trends may differentiate random and trait-selective mass extinctions, but methods struggle to identify trait selectivity. Long-term effects of mass extinction trait selectivity change support for phylogenetic comparative methods away from the simulated Brownian motion toward Ornstein-Uhlenbeck and Early Burst models. We find that morphological change over mass extinction is best studied by quantifying multiple aspects of morphospace occupation.

Rates of ecomorphological trait evolution in passerine bird clades are independent of age

Abstract Although the links between species richness and diversification rates with clade age have been studied extensively, few studies have investigated the relationship between the rates of trait evolution and clade age. The rate of morphological trait evolution has repeatedly been shown to vary through time, as expected, for example, for adaptive radiations, but the strength and sources of this variation are not well understood. We compare the relationship between the rates of trait evolution and clade age across eight monophyletic clades of passerine birds by investigating ecomorphological traits, i.e. morphological traits that influence the ecology of the species directly. We study the ecomorphological divergence pattern using analyses of the disparity through time and determine the best-fitting model of evolution for each trait in each clade. We find no support for a consistent dependence of evolutionary rates on clade age across wing, tail, tarsus and beak shape in our eight clades and also show that early burst models of trait evolution are rarely the best-fitting models within these clades. These results suggest that key innovations or adaptive radiations might be less common evolutionary patterns and processes than generally thought or might depend on the taxonomic level investigated.

Repeated evolution of terrestrial lineages in a continental lizard radiation.

The "early-burst" model of adaptive radiation predicts an early increase in phenotypic disparity concurrent with lineage diversification. Although most studies report a lack of this coupled pattern, the underlying processes are not identified. The continental radiation of Hemidactylus geckos from Peninsular India includes morphologically diverse species that occupy various microhabitats. This radiation began diversifying ~36Mya with an early increase in lineage diversification. Here, we test the "early-burst" hypothesis by investigating the presence of ecomorphs and examining the pattern of morphological diversification in a phylogenetic framework. Two ecomorphs-terrestrial and scansorial species-that vary significantly in body size and toepad size were identified. Unlike the prediction of the "early-burst" model, we find that disparity in toepad morphology accumulated more recently ~14Mya and fit the Ornstein-Ulhenbeck model. Ancestral state reconstruction of the two ecomorphs demonstrates that terrestrial lineages evolved independently at least five times from scansorial ancestors, with the earliest diversification in terrestrial lineages 19-12Mya. Our study demonstrates a delayed increase in morphological disparity as a result of the evolution of terrestrial ecomorphs. The diversification of terrestrial lineages is concurrent with the establishment of open habitat and grasslands in Peninsular India, suggesting that the appearance of this novel resource led to the adaptive diversification.

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 levelclades.

A Penalized Likelihood Framework for High-Dimensional Phylogenetic Comparative Methods and an Application to New-World Monkeys Brain Evolution.

Working with high-dimensional phylogenetic comparative data sets is challenging because likelihood-based multivariate methods suffer from low statistical performances as the number of traits $p $ approaches the number of species $n $ and because some computational complications occur when $p $ exceeds $n$. Alternative phylogenetic comparative methods have recently been proposed to deal with the large $p $ small $n $ scenario but their use and performances are limited. Herein, we develop a penalized likelihood (PL) framework to deal with high-dimensional comparative data sets. We propose various penalizations and methods for selecting the intensity of the penalties. We apply this general framework to the estimation of parameters (the evolutionary trait covariance matrix and parameters of the evolutionary model) and model comparison for the high-dimensional multivariate Brownian motion (BM), Early-burst (EB), Ornstein-Uhlenbeck (OU), and Pagel's lambda models. We show using simulations that our PL approach dramatically improves the estimation of evolutionary trait covariance matrices and model parameters when $p$ approaches $n$, and allows for their accurate estimation when $p$ equals or exceeds $n$. In addition, we show that PL models can be efficiently compared using generalized information criterion (GIC). We implement these methods, as well as the related estimation of ancestral states and the computation of phylogenetic principal component analysis in the R package RPANDA and mvMORPH. Finally, we illustrate the utility of the new proposed framework by evaluating evolutionary models fit, analyzing integration patterns, and reconstructing evolutionary trajectories for a high-dimensional 3D data set of brain shape in the New World monkeys. We find a clear support for an EB model suggesting an early diversification of brain morphology during the ecological radiation of the clade. PL offers an efficient way to deal with high-dimensional multivariate comparative data.

Evolution of jaw disparity in fishes

AbstractThe morphology of the vertebrate lower jaw has been used to infer feeding ecology, with transformations in mandibular shape and structure likely to have facilitated the emergence of different feeding behaviours in vertebrate evolution. Here we present elliptical Fourier shape and principal component analyses, characterizing and comparing the disparity of jaw shape in early gnathostomes and their modern primitively aquatic counterparts. 83% of shape variation is summarized on the first three principal component axes and all component clades of early gnathostomes exhibit overlapping morphological variation. Non‐tetrapodomorph Palaeozoic sarcopterygians are more disparate than their extant counterparts whereas extant chondrichthyans are more disparate than their Palaeozoic counterparts. More generally, extant jawed fishes are more disparate than their Palaeozoic relatives largely because of the extensive shape variation exhibited by mandibles of extant actinopterygians. Only some areas of shape space vacated by Palaeozoic gnathostomes have been convergently refilled by living taxa. Characterization of theoretical jaw morphologies demonstrates that fewer than half of all possible shapes are realized by the jawed fishes that comprise our empirical dataset; many of these morphologies are realized by unrepresented terrestrial tetrapods, implying environmental constraint. Our results are incompatible with the early burst model of clade evolution and contradict the hypothesis that maximum disparity is reached early in the evolutionary history of jawed fishes.

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.

Mixed evidence for early bursts of morphological evolution in extant clades.

Macroevolutionary theory predicts high rates of evolution should occur early in a clade's history as species exploit ecological opportunity. Evidence from the fossil record has shown a high prevalence of early bursts in morphological evolution, but recent work has provided little evidence for early high rates in the evolution of extant clades. Here, I test the prevalence of early bursts in extant data using phylogenetic comparative methods. Existing models are extended to allow a shift from a background Brownian motion (BM) process to an early burst process within subclades of phylogenies, rather than an early burst being applied to an entire phylogenetic tree. This nested early burst model is compared to other modes of evolution that can occur within subclades, such as evolution with a constraint (Ornstein‐Uhlenbeck model) and nested BM rate shift models. These relaxed models are validated using simulations and then are applied to body size evolution of three major clades of amniotes (mammals, squamates and aves) at different levels of taxonomic organization (order, family). Applying these unconstrained models greatly increases the support for early bursts within nested subclades, and so early bursts are the most common model of evolution when only one shift is analysed. However, the relative fit of early burst models is worse than models that allow for multiple shifts of the BM or OU process. No single‐shift or homogenous model is superior to models of multiple shifts in BM or OU evolution, but the patterns shown by these multirate models are generally congruent with patterns expected from early bursts.

Trait Evolution in Adaptive Radiations: Modeling and Measuring Interspecific Competition on Phylogenies.

The incorporation of ecological processes into models of trait evolution is important for understanding past drivers of evolutionary change. Species interactions have long been thought to be key drivers of trait evolution. However, models for comparative data that account for interactions between species are lacking. One of the challenges is that such models are intractable and difficult to express analytically. Here we present phylogenetic models of trait evolution that include interspecific competition among chosen species. Competition is modeled as a tendency of sympatric species to evolve toward difference from one another, producing trait overdispersion and high phylogenetic signal. The model predicts elevated trait variance across species and a slowdown in evolutionary rate both across the clade and within each branch. The model also predicts a reduction in correlation between otherwise correlated traits. We use an approximate Bayesian computation approach to estimate model parameters. We find reasonable power to detect competition in sufficiently large (20+ species) trees compared with Brownian trait evolution and with Ornstein-Uhlenbeck and early burst models. We apply the model to examine the evolution of bill morphology of Darwin's finches and find evidence that competition affects the evolution of bill length.

Limited role of functional differentiation in early diversification of animals.

The origin of most animal phyla and classes during the Cambrian explosion has been hypothesized to represent an ‘early burst’ of evolutionary exploration of functional ecological possibilities. However, the ecological history of marine animals has yet to be fully quantified, preventing an assessment of the early-burst model for functional ecology. Here we use ecological assignments for 18,621 marine animal genera to assess the relative timing of functional differentiation versus taxonomic diversification from the Cambrian to the present day. We find that functional diversity increased more slowly than would be expected given the history of taxonomic diversity. Contrary to previous inferences of rapid ecological differentiation from the early appearances of all well-fossilized phyla and classes, explicit coding of functional characteristics demonstrates that Cambrian genera occupied comparatively few modes of life. Functional diversity increased in the Ordovician and, especially, during the recoveries from the end-Permian and end-Cretaceous mass extinctions. Permanent shifts in the relationship between functional and taxonomic diversity following the era-bounding extinctions indicates a critical role for these biotic crises in coupling taxonomic and functional diversity.

Experimental evidence that the Ornstein-Uhlenbeck model best describes the evolution of leaf litter decomposability.

Leaf litter decomposability is an important effect trait for ecosystem functioning. However, it is unknown how this effect trait evolved through plant history as a leaf ‘afterlife’ integrator of the evolution of multiple underlying traits upon which adaptive selection must have acted. Did decomposability evolve in a Brownian fashion without any constraints? Was evolution rapid at first and then slowed? Or was there an underlying mean-reverting process that makes the evolution of extreme trait values unlikely? Here, we test the hypothesis that the evolution of decomposability has undergone certain mean-reverting forces due to strong constraints and trade-offs in the leaf traits that have afterlife effects on litter quality to decomposers. In order to test this, we examined the leaf litter decomposability and seven key leaf traits of 48 tree species in the temperate area of China and fitted them to three evolutionary models: Brownian motion model (BM), Early burst model (EB), and Ornstein-Uhlenbeck model (OU). The OU model, which does not allow unlimited trait divergence through time, was the best fit model for leaf litter decomposability and all seven leaf traits. These results support the hypothesis that neither decomposability nor the underlying traits has been able to diverge toward progressively extreme values through evolutionary time. These results have reinforced our understanding of the relationships between leaf litter decomposability and leaf traits in an evolutionary perspective and may be a helpful step toward reconstructing deep-time carbon cycling based on taxonomic composition with more confidence.

A Linear-Time Algorithm for Gaussian and Non-Gaussian Trait Evolution Models

We developed a linear-time algorithm applicable to a large class of trait evolution models, for efficient likelihood calculations and parameter inference on very large trees. Our algorithm solves the traditional computational burden associated with two key terms, namely the determinant of the phylogenetic covariance matrix V and quadratic products involving the inverse of V. Applications include Gaussian models such as Brownian motion-derived models like Pagel's lambda, kappa, delta, and the early-burst model; Ornstein-Uhlenbeck models to account for natural selection with possibly varying selection parameters along the tree; as well as non-Gaussian models such as phylogenetic logistic regression, phylogenetic Poisson regression, and phylogenetic generalized linear mixed models. Outside of phylogenetic regression, our algorithm also applies to phylogenetic principal component analysis, phylogenetic discriminant analysis or phylogenetic prediction. The computational gain opens up new avenues for complex models or extensive resampling procedures on very large trees. We identify the class of models that our algorithm can handle as all models whose covariance matrix has a 3-point structure. We further show that this structure uniquely identifies a rooted tree whose branch lengths parametrize the trait covariance matrix, which acts as a similarity matrix. The new algorithm is implemented in the R package phylolm, including functions for phylogenetic linear regression and phylogenetic logistic regression.

Convergences and Trends in the Evolution of the Archosaur Pelvis

The pelvic structure in non-avian archosaurs plays a key role in understanding the evolution of terrestrial locomotor patterns because the pelvis contains major attachment sites for proximal hind limb musculature. In order to investigate patterns of pelvic evolution in archosaurs, this study compiled three pelvic indices, as well as femoral head orientation, for 92 archosaur taxa. With the metrics and a reconstructed supertree, we examined the correlated evolution of the pelvis and femur, the correlation among pelvic components, and temporal trends in the evolution of the pelvis. The result shows that archosaurs with medially directed femoral heads have more cranially shifted iliac centroids and more posteriorly rotated pubes than taxa with anteromedially directed femoral heads. The craniad shift of the iliac centroid might be correlated to the posterior rotation of pubis. The pelvic structures of pterosaurs, ornithischians, sauropods, and avetheropods occupy a different morphospace from basal archosaurs, pseudosuchians, basal dinosauromorphs, basal theropods, and basal sauropodomorphs in having more cranially expanded ilia, more posteriorly rotated pubes, and medially deflected femoral heads. This may imply that pterosaurs and those derived dinosaurs independently underwent similar shifts in thigh muscles and locomotion. The evolutionary model fitting supports the early-burst model for iliac and pubic metrics in more inclusive archosaur clades, indicating that larger changes of archosaur pelves occurred in early times of the clade's history.

Robust Regression and Posterior Predictive Simulation Increase Power to Detect Early Bursts of Trait Evolution

A central prediction of much theory on adaptive radiations is that traits should evolve rapidly during the early stages of a clade's history and subsequently slowdown in rate as niches become saturated--a so-called "Early Burst." Although a common pattern in the fossil record, evidence for early bursts of trait evolution in phylogenetic comparative data has been equivocal at best. We show here that this may not necessarily be due to the absence of this pattern in nature. Rather, commonly used methods to infer its presence perform poorly when when the strength of the burst--the rate at which phenotypic evolution declines--is small, and when some morphological convergence is present within the clade. We present two modifications to existing comparative methods that allow greater power to detect early bursts in simulated datasets. First, we develop posterior predictive simulation approaches and show that they outperform maximum likelihood approaches at identifying early bursts at moderate strength. Second, we use a robust regression procedure that allows for the identification and down-weighting of convergent taxa, leading to moderate increases in method performance. We demonstrate the utility and power of these approach by investigating the evolution of body size in cetaceans. Model fitting using maximum likelihood is equivocal with regards the mode of cetacean body size evolution. However, posterior predictive simulation combined with a robust node height test return low support for Brownian motion or rate shift models, but not the early burst model. While the jury is still out on whether early bursts are actually common in nature, our approach will hopefully facilitate more robust testing of this hypothesis. We advocate the adoption of similar posterior predictive approaches to improve the fit and to assess the adequacy of macroevolutionary models in general.