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.     

Exploring the tempo of species diversification in legumes

Whatever criteria are used to measure evolutionary success – species numbers, geographic range, ecological abundance, ecological and life history diversity, background diversification rates, or the presence of rapidly evolving clades – the legume family is one of the most successful lineages of flowering plants. Despite this, we still know rather little about the dynamics of lineage and species diversification across the family through the Cenozoic, or about the underlying drivers of diversification. There have been few attempts to estimate net species diversification rates or underlying speciation and extinction rates for legume clades, to test whether among-lineage variation in diversification rates deviates from null expectations, or to locate species diversification rate shifts on specific branches of the legume phylogenetic tree. In this study, time-calibrated phylogenetic trees for a set of species-rich legume clades – Calliandra, Indigofereae, Lupinus, Mimosa and Robinieae – and for the legume family as a whole, are used to explore how we might approach these questions. These clades are analysed using recently developed maximum likelihood and Bayesian methods to detect species diversification rate shifts and test for among-lineage variation in speciation, extinction and net diversification rates. Possible explanations for rate shifts in terms of extrinsic factors and/or intrinsic trait evolution are discussed. In addition, several methodological issues and limitations associated with these analyses are highlighted emphasizing the potential to improve our understanding of the evolutionary dynamics of legume diversification by using much more densely sampled phylogenetic trees that integrate information across broad taxonomic, geographical and temporal levels.     

Phylogenetic estimates of diversification rate are affected by molecular rate variation

Molecular phylogenies are increasingly being used to investigate the patterns and mechanisms of macroevolution. In particular, node heights in a phylogeny can be used to detect changes in rates of diversification over time. Such analyses rest on the assumption that node heights in a phylogeny represent the timing of diversification events, which in turn rests on the assumption that evolutionary time can be accurately predicted from DNA sequence divergence. But there are many influences on the rate of molecular evolution, which might also influence node heights in molecular phylogenies, and thus affect estimates of diversification rate. In particular, a growing number of studies have revealed an association between the net diversification rate estimated from phylogenies and the rate of molecular evolution. Such an association might, by influencing the relative position of node heights, systematically bias estimates of diversification time. We simulated the evolution of DNA sequences under several scenarios where rates of diversification and molecular evolution vary through time, including models where diversification and molecular evolutionary rates are linked. We show that commonly used methods, including metric‐based, likelihood and Bayesian approaches, can have a low power to identify changes in diversification rate when molecular substitution rates vary. Furthermore, the association between the rates of speciation and molecular evolution rate can cause the signature of a slowdown or speedup in speciation rates to be lost or misidentified. These results suggest that the multiple sources of variation in molecular evolutionary rates need to be considered when inferring macroevolutionary processes from phylogenies.     

How important is it to consider lineage diversification heterogeneity in macroevolutionary studies? Lessons from the lizard family Liolaemidae

Macroevolutionary and biogeographical studies commonly apply multiple models to test state-dependent diversification. These models track the association between states of interest along a phylogeny, although many of them do not consider whether different clades might be evolving under different evolutionary drivers. Yet, they are still commonly applied to empirical studies without careful consideration of possible lineage diversification heterogeneity along the phylogenetic tree. A recent biogeographic study has suggested that orogenic uplift of the southern Andes has acted as a species pump, driving diversification of the lizard family Liolaemidae (307 described species), native to temperate southern South America. Here, we argue against the Andean uplift as main driver of evolution in this group. We show that there is a clear pattern of heterogeneous diversification in the Liolaemidae, which biases state- and environment-dependent analyses in, respectively, the GeoSSE and RPANDA programs. We show here that there are two shifts to accelerated speciation rates involving two clades that have both been classified as having “Andean” distributions. We incorporated the Geographic Hidden-State Speciation and Extinction model (GeoHiSSE) to accommodate unrelated diversification shifts, and also re-analyzed the data in RPANDA program after splitting biologically distinct clades for separate analyses, as well as including a more appropriate set of models. We demonstrate that the “Andean uplift” hypothesis is not supported when the heterogeneous diversification histories among these lizards is considered. We use the Liolaemidae as an ideal system to demonstrate potential risks of ignoring clade-specific differences in diversification patterns in macroevolutionary studies. We also implemented simulations to show that, in agreement with previous findings, the HiSSE approach can effectively and substantially reduce the level of distribution-dependent models receiving the highest AIC weights in such scenarios. However, we still find a relatively high rate (15%) of distribution-dependent models receiving the highest AIC weights, and provide recommendations related to the set of models included in the analyses that reduce these rates by half. Finally, we demonstrate that trees including clades following different dependent-drivers affect RPANDA analyses by producing different outcomes, ranging from partially correct models to completely misleading results. We provide recommendations for the implementation of both programs.     

Evolution of floral morphology and pollination system in Bignonieae (Bignoniaceae)

The radiation of angiosperms is associated with shifts among pollination modes that are thought to have driven the diversification of floral forms. However, the exact sequence of evolutionary events that led to such great diversity in floral traits is unknown for most plant groups. Here, we characterize the patterns of evolution of individual floral traits and overall floral morphologies in the tribe Bignonieae (Bignoniaceae). We identified 12 discrete traits that are associated with seven floral types previously described for the group and used a penalized likelihood tree of the tribe to reconstruct the ancestral states of those traits at all nodes of the phylogeny of Bignonieae. In addition, evolutionary correlations among traits were conducted using a maximum likelihood approach to test whether the evolution of individual floral traits followed the correlated patterns of evolution expected under the "pollination syndrome" concept. The ancestral Bignonieae flower presented an Anemopaegma-type morphology, which was followed by several parallel shifts in floral morphologies. Those shifts occurred through intermediate stages resulting in mixed floral morphologies as well as directly from the Anemopaegma-type morphology to other floral types. Positive and negative evolutionary correlations among traits fit patterns expected under the pollination syndrome perspective, suggesting that interactions between Bignonieae flowers and pollinators likely played important roles in the diversification of the group as a whole.     

Identifying heterogeneity in rates of morphological evolution: discrete character change in the evolution of lungfish (Sarcopterygii; Dipnoi)

Quantifying rates of morphological evolution is important in many macroevolutionary studies, and critical when assessing possible adaptive radiations and episodes of punctuated equilibrium in the fossil record. However, studies of morphological rates of change have lagged behind those on taxonomic diversification, and most authors have focused on continuous characters and quantifying patterns of morphological rates over time. Here, we provide a phylogenetic approach, using discrete characters and three statistical tests to determine points on a cladogram (branches or entire clades) that are characterized by significantly high or low rates of change. These methods include a randomization approach that identifies branches with significantly high rates and likelihood ratio tests that pinpoint either branches or clades that have significantly higher or lower rates than the pooled rate of the remainder of the tree. As a test case for these methods, we analyze a discrete character dataset of lungfish, which have long been regarded as "living fossils" due to an apparent slowdown in rates since the Devonian. We find that morphological rates are highly heterogeneous across the phylogeny and recover a general pattern of decreasing rates along the phylogenetic backbone toward living taxa, from the Devonian until the present. Compared with previous work, we are able to report a more nuanced picture of lungfish evolution using these new methods.     

Ecological opportunity alters the timing and shape of adaptive radiation

The uneven distribution of diversity is a conspicuous phenomenon across the tree of life. Ecological opportunity is a prominent catalyst of adaptive radiation and therefore may alter patterns of diversification. We evaluated the distribution of shifts in diversification rates across the cichlid phylogeny and the distribution of major clades across phylogenetic space. We also tested if ecological opportunity influenced these patterns. Colonization‐associated ecological opportunity altered the tempo and mode of diversification during the adaptive radiation of cichlid fishes. Clades that arose following colonization events diversified faster than other clades. Speciation rate shifts were nonrandomly distributed across the phylogeny such that they were disproportionally concentrated around nodes that corresponded with colonization events (i.e., of continents, river basins, or lakes). Young clades tend to expand faster than older clades; however, colonization‐associated ecological opportunity accentuated this pattern. There was an interaction between clade age and ecological opportunity that explained the trajectory of clades through phylogenetic space over time. Our results indicate that ecological opportunities afforded by continental and ecosystem‐scale colonization events explain the dramatic speciation rate heterogeneity and phylogenetic imbalance that arose during the evolutionary history of cichlid fishes.     

Diversification rates in the Australasian endemic grass <Emphasis Type="Italic">Austrostipa</Emphasis>: 15 million years of constant evolution

Patterns seen in other Australian flora have led to hypotheses that early Miocene shifts in climate drove rapid radiation of major taxonomic groups such as Eucalyptus. Little is known about absolute dates and rates for Australian monocots, particularly grasses. I tested this early Miocene radiation hypothesis for Australian grasses using a calibrated phylogeny of the endemic stipoid genus Austrostipa and an analysis of diversification rates. The phylogeny was developed from a Bayesian likelihood analysis of the nuclear internal transcribed spacers region, and three calibration points were set based on fossil evidence. The results indicate that the genus arose in the early Miocene and underwent a species radiation, but the rate of diversification was not rapid compared to the current rate or to those of other taxa. Following an 8 million year period of fast molecular evolution but no taxonomic radiation, diversification rates have been constant for the past 15 million years. Comparable measures such as the gamma statistic can be used across taxa to make general conclusions about evolutionary rate constancy.     

Misinformative characters and phylogeny shape

The discrepancy between theoretical and observed distributions of tree shapes in recent surveys of phylogeny estimates has lead to investigations of possible biological and methodological causes. I investigated whether the phylogenetic quality of characters is related to the tree shape on which they evolve. Simulated evolution revealed shape-related tendencies for characters to indicate correct cladistic relationships; these differences were measured by examining the characters directly, without deriving any phylogeny estimates. Tree stemminess indices correlated strongly with character quality when characters evolved either speciationally or phyletically. Tree balance was a significant correlate of character quality under speciational evolution but not under phyletic evolution. These results help explain the findings of other simulation studies. With additional study of the behavior of evolving characters and their interaction with phylogenetic methods, we might be able to increase the accuracy of tree estimation and compensate for potential biases related to shape. These results give further reason for caution in trusting phylogeny estimates.     

Ecological and Ecomorphological Specialization Are Not Associated with Diversification Rates in Muroid Rodents (Rodentia: Muroidea)

Multiple diversification rate shifts explain uneven clade richness in muroid rodents. Previous muroid studies have shown that extrinsic factors, notwithstanding ecological opportunity, are poor predictors of clade diversity. Here, we use a 297-muroid species chronogram that is sampled proportional to total clade diversity, along with various trait-dependent diversification approaches to investigate the association between diversification rates with intrinsic attributes—diet, habitat, body mass, and relative tail length. We found some association between both dietary specialization and body mass, as well as between habitat specialization with relative tail lengths using phylogenetic analyses of variance. However, there was no significant association between diversification rates with the evolution of these traits in muroid rodents. We also show that several of the state-dependent diversification approaches are highly susceptible to Type I error—a result that is in accordance with recent criticisms of these methods. Finally, we discuss several potential causes for the lack of association between the examined trait data with diversification rates, ranging from methodological biases (e.g. method conservativism) to biology (e.g. behavioral plasticity and ecological opportunism of muroid rodents).     

SYMMETREE: whole-tree analysis of differential diversification rates

SymmeTREE implements several tests of differential diversification rates that exploit information on the topological distribution of species diversity throughout entire trees to address two general questions: (1) Has a given tree experienced significant variation in diversification rates among its branches? and (2) If so, along which branches have significant shifts in diversification rate occurred? These explicitly model-based methods are robust to uncertainty in estimates of branch length/duration and can accommodate incompletely resolved trees and other forms of phylogenetic uncertainty. AVAILABILITY: http://www.phylodiversity.net/bmoore/software.html CONTACT: brian.moore@yale.edu.     

Corolla morphology influences diversification rates in bifid toadflaxes (Linaria sect. Versicolores)

Background and Aims

The role of flower specialization in plant speciation and evolution remains controversial. In this study the evolution of flower traits restricting access to pollinators was analysed in the bifid toadflaxes (Linaria sect. Versicolores), a monophyletic group of ∼30 species and subspecies with highly specialized corollas.

Methods

A time-calibrated phylogeny based on both nuclear and plastid DNA sequences was obtained using a coalescent-based method, and flower morphology was characterized by means of morphometric analyses. Directional trends in flower shape evolution and trait-dependent diversification rates were jointly analysed using recently developed methods, and morphological shifts were reconstructed along the phylogeny. Pollinator surveys were conducted for a representative sample of species.

Key Results

A restrictive character state (narrow corolla tube) was reconstructed in the most recent common ancestor of Linaria sect. Versicolores. After its early loss in the most species-rich clade, this character state has been convergently reacquired in multiple lineages of this clade in recent times, yet it seems to have exerted a negative influence on diversification rates. Comparative analyses and pollinator surveys suggest that the narrow- and broad-tubed flowers are evolutionary optima representing divergent strategies of pollen placement on nectar-feeding insects.

Conclusions

The results confirm that different forms of floral specialization can lead to dissimilar evolutionary success in terms of diversification. It is additionally suggested that opposing individual-level and species-level selection pressures may have driven the evolution of pollinator-restrictive traits in bifid toadflaxes.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

Evolutionary patterns in early tetrapods. I. Rapid initial diversification followed by decrease in rates of character change

Although numerous studies have examined morphological diversification during major radiations of marine taxa, much less attention has been paid to terrestrial radiations. Here, we examine rates of character change over phylogeny and over time for Palaeozoic limbed tetrapods. Palaeozoic tetrapods show significant decreases in rates of character change whether the rate is measured per sampled cladistic branch or per million years along phylogeny. Given changes per branch, rates decrease significantly from the Devonian through the Pennsylvanian, but not from the Pennsylvanian through the Permian. Given changes per million years, rates decrease significantly over each boundary, although the decrease is least significant over the Pennsylvanian-Permian boundary. Decreasing rates per million years through the Permian might be an artefact of the method being able to ascribe longer durations to Permian branches than to Carboniferous ones; however, it is difficult to ascribe the general pattern of decreasing rates of change over time to sampling biases or methodological biases. Thus, the results implicate biological explanations for this pattern.     

Developmental life history is associated with variation in rates of climatic niche evolution in a salamander adaptive radiation*

Rates of climatic niche evolution vary widely across the tree of life and are strongly associated with rates of diversification among clades. However, why the climatic niche evolves more rapidly in some clades than others remains unclear. Variation in life history traits often plays a key role in determining the environmental conditions under which species can survive, and therefore, could impact the rate at which lineages can expand in available climatic niche space. Here, we explore the relationships among life-history variation, climatic niche breadth, and rates of climatic niche evolution. We reconstruct a phylogeny for the genus Desmognathus, an adaptive radiation of salamanders distributed across eastern North America, based on nuclear and mitochondrial genes. Using this phylogeny, we estimate rates of climatic niche evolution for species with long, short, and no aquatic larval stage. Rates of climatic niche evolution are unrelated to the mean climatic niche breadth of species with different life histories. Instead, we find that the evolution of a short larval period promotes greater exploration of climatic space, leading to increased rates of climatic niche evolution across species having this trait. We propose that morphological and physiological differences associated with variation in larval stage length underlie the heterogeneous ability of lineages to explore climatic niche space. Rapid rates of climatic niche evolution among species with short larval periods were an important dimension of the clade's adaptive radiation and likely contributed to the rapid rate of lineage accumulation following the evolution of an aquatic life history in this clade. Our results show how variation in a key life-history trait can constrain or promote divergence of the climatic niche, leading to variation in rates of climatic niche evolution among species.     

A novel comparative method for identifying shifts in the rate of character evolution on trees

Evolutionary biologists since Darwin have been fascinated by differences in the rate of trait-evolutionary change across lineages. Despite this continued interest, we still lack methods for identifying shifts in evolutionary rates on the growing tree of life while accommodating uncertainty in the evolutionary process. Here we introduce a Bayesian approach for identifying complex patterns in the evolution of continuous traits. The method (auteur) uses reversible-jump Markov chain Monte Carlo sampling to more fully characterize the complexity of trait evolution, considering models that range in complexity from those with a single global rate to potentially ones in which each branch in the tree has its own independent rate. This newly introduced approach performs well in recovering simulated rate shifts and simulated rates for datasets nearing the size typical for comparative phylogenetic study (i.e., ≥64 tips). Analysis of two large empirical datasets of vertebrate body size reveal overwhelming support for multiple-rate models of evolution, and we observe exceptionally high rates of body-size evolution in a group of emydid turtles relative to their evolutionary background. auteur will facilitate identification of exceptional evolutionary dynamics, essential to the study of both adaptive radiation and stasis.     

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.     

Rates of morphological evolution are correlated with species richness in salamanders

The tempo and mode of species diversification and phenotypic evolution vary widely across the tree of life, yet the relationship between these processes is poorly known. Previous tests of the relationship between rates of phenotypic evolution and rates of species diversification have assumed that species richness increases continuously through time. If this assumption is violated, simple phylogenetic estimates of net diversification rate may bear no relationship to processes that influence the distribution of species richness among clades. Here, we demonstrate that the variation in species richness among plethodontid salamander clades is unlikely to have resulted from simple time-dependent processes, leading to fundamentally different conclusions about the relationship between rates of phenotypic evolution and species diversification. Morphological evolutionary rates of both size and shape evolution are correlated with clade species richness, but are uncorrelated with simple estimators of net diversification that assume constancy of rates through time. This coupling between species diversification and phenotypic evolution is consistent with the hypothesis that clades with high rates of morphological trait evolution may diversify more than clades with low rates. Our results indicate that assumptions about underlying processes of diversity regulation have important consequences for interpreting macroevolutionary patterns.     

Colonization history, ecological shifts and diversification in the evolution of endemic Galápagos weevils

Mitochondrial DNA sequence data were obtained for eight species of flightless Galapaganus endemic weevils and one winged close relative in order to study their colonization history and modes of diversification in the Galápagos Archipelago. Contrary to most other insular radiations, the phylogeny estimates we recovered for Galapaganus do not follow the progression rule of island biogeography. The penalized likelihood age estimates of colonization of the archipelago exceed the age of the emerged islands and underscore the potential role of now sunken seamounts for the early evolution of Galapaganus . The phylogeny proposes one intra-island origin for Galapaganus endemics, but monophyly tests suggest a larger contribution of in-situ speciation on older islands. Generalist habitat preferences were reconstructed as ancestral while shifts to highland habitats were reconstructed as having evolved independently on different islands. Magnitudes and patterns of diversification rate were found to differ between older and younger islands. Our analyses reveal that the colonization sequence of islands and timing of colonization of Galapaganus could be linked with the geological and volcanic history of the islands in a rather complex scenario. Even though most islands appear to have been colonized soon after their emergence, there are notable deviations from the pattern of sequential colonization expected under the progression rule when considering only the extant emerged islands. Patterns of diversification rate variation on older and younger islands correspond to the volcanic activity or remnants of such activity, while the pattern of independent evolution of restricted habitat preferences in different islands suggests that habitat shifts could also have contributed to species diversity in Galapaganus .     

An approach of orthology detection from homologous sequences under minimum evolution

In the field of phylogenetics and comparative genomics, it is important to establish orthologous relationships when comparing homologous sequences. Due to the slight sequence dissimilarity between orthologs and paralogs, it is prone to regarding paralogs as orthologs. For this reason, several methods based on evolutionary distance, phylogeny and BLAST have tried to detect orthologs with more precision. Depending on their algorithmic implementations, each of these methods sometimes has increased false negative or false positive rates. Here, we developed a novel algorithm for orthology detection that uses a distance method based on the phylogenetic criterion of minimum evolution. Our algorithm assumes that sets of sequences exhibiting orthologous relationships are evolutionarily less costly than sets that include one or more paralogous relationships. Calculation of evolutionary cost requires the reconstruction of a neighbor-joining (NJ) tree, but calculations are unaffected by the topology of any given NJ tree. Unlike tree reconciliation, our algorithm appears free from the problem of incorrect topologies of species and gene trees. The reliability of the algorithm was tested in a comparative analysis with two other orthology detection methods using 95 manually curated KOG datasets and 21 experimentally verified EXProt datasets. Sensitivity and specificity estimates indicate that the concept of minimum evolution could be valuable for the detection of orthologs.