EXTINCTION RATES SHOULD NOT BE ESTIMATED FROM MOLECULAR PHYLOGENIES

Molecular phylogenies contain information about the tempo and mode of species diversification through time. Because extinction leaves a characteristic signature in the shape of molecular phylogenetic trees, many studies have used data from extant taxa only to infer extinction rates. This is a promising approach for the large number of taxa for which extinction rates cannot be estimated from the fossil record. Here, I explore the consequences of violating a common assumption made by studies of extinction from phylogenetic data. I show that when diversification rates vary among lineages, simple estimators based on the birth–death process are unable to recover true extinction rates. This is problematic for phylogenetic trees with complete taxon sampling as well as for the simpler case of clades with known age and species richness. Given the ubiquity of variation in diversification rates among lineages and clades, these results suggest that extinction rates should not be estimated in the absence of fossil data.     

Minimal effects of latitude on present-day speciation rates in New World birds

The tropics contain far greater numbers of species than temperate regions, suggesting that rates of species formation might differ systematically between tropical and non-tropical areas. We tested this hypothesis by reconstructing the history of speciation in New World (NW) land birds using BAMM, a Bayesian framework for modelling complex evolutionary dynamics on phylogenetic trees. We estimated marginal distributions of present-day speciation rates for each of 2571 species of birds. The present-day rate of speciation varies approximately 30-fold across NW birds, but there is no difference in the rate distributions for tropical and temperate taxa. Using macroevolutionary cohort analysis, we demonstrate that clades with high tropical membership do not produce species more rapidly than temperate clades. For nearly any value of present-day speciation rate, there are far more species in the tropics than the temperate zone. Any effects of latitude on speciation rate are marginal in comparison to the dramatic variation in rates among clades.     

QUANTIFYING VARIATION IN SPECIATION AND EXTINCTION RATES WITH CLADE DATA

High‐level phylogenies are very common in evolutionary analyses, although they are often treated as incomplete data. Here, we provide statistical tools to analyze what we name “clade data,” which are the ages of clades together with their numbers of species. We develop a general approach for the statistical modeling of variation in speciation and extinction rates, including temporal variation, unknown variation, and linear and nonlinear modeling. We show how this approach can be generalized to a wide range of situations, including testing the effects of life‐history traits and environmental variables on diversification rates. We report the results of an extensive simulation study to assess the performance of some statistical tests presented here as well as of the estimators of speciation and extinction rates. These latter results suggest the possibility to estimate correctly extinction rate in the absence of fossils. An example with data on fish is presented.     

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.     

Dynamic diversification history with rate upshifts in Holarctic bell‐flowers (Campanula and allies)

Campanula s.l. is one of the most speciose flowering plant lineages of the Holarctic (ca. 600 species). In the present study we sequenced three regions of the plastid genome (petD, rpl16 and trnK/matK) across a broad sample of Campanula s.l., which markedly improved phylogenetic resolution and statistical support compared to previous studies. Based on this robust phylogenetic hypothesis we estimated divergence times using BEAST, diversification rate shifts using Bayesian Analysis of Macroevolutionary Mixture (BAMM) and TreePar, and ancestral ranges using Biogeography with Bayesian (and likelihood) Evolutionary Analyses in R. Campanula s.l. is estimated to have originated during the Early Eocene but the major diversification events occurred between the Late Oligocene and Middle Miocene. Two upward diversification rate shifts were revealed by BAMM, specific to the crown nodes of two Campanula clades: CAM17, a mostly South European‐SW Asian lineage originating during the Middle Miocene and containing nearly half of all known Campanula species; and CAM15B, a SW Asian–Sino‐Himalayan lineage of nine species originating in the early Pleistocene. The dynamic diversification history of Campanula and the inferred rate shifts are discussed in a geo‐historical context.     

ABSOLUTE DIVERSIFICATION RATES IN ANGIOSPERM CLADES

Abstract The extraordinary contemporary species richness and ecological predominance of flowering plants (angiosperms) are even more remarkable when considering the relatively recent onset of their evolutionary diversification. We examine the evolutionary diversification of angiosperms and the observed differential distribution of species in angiosperm clades by estimating the rate of diversification for angiosperms as a whole and for a large set of angiosperm clades. We also identify angiosperm clades with a standing diversity that is either much higher or lower than expected, given the estimated background diversification rate. Recognition of angiosperm clades, the phylogenetic relationships among them, and their taxonomic composition are based on an empirical compilation of primary phylogenetic studies. By making an integrative and critical use of the paleobotanical record, we obtain reasonably secure approximations for the age of a large set of angiosperm clades. Diversification was modeled as a stochastic, time‐homogeneous birth‐and‐death process that depends on the diversification rate (r) and the relative extinction rate (∈). A statistical analysis of the birth and death process was then used to obtain 95% confidence intervals for the expected number of species through time in a clade that diversifies at a rate equal to that of angiosperms as a whole. Confidence intervals were obtained for stem group and for crown group ages in the absence of extinction (∈= 0.0) and under a high relative extinction rate (∈= 0.9). The standing diversity of angiosperm clades was then compared to expected species diversity according to the background rate of diversification, and, depending on their placement with respect to the calculated confidence intervals, exceedingly species‐rich or exceedingly species‐poor clades were identified. The rate of diversification for angiosperms as a whole ranges from 0.077 (∈= 0.9) to 0.089 (∈= 0.0) net speciation events per million years. Ten clades fall above the confidence intervals of expected species diversity, and 13 clades were found to be unexpectedly species poor. The phylogenetic distribution of clades with an exceedingly high number of species suggests that traits that confer high rates of diversification evolved independently in different instances and do not characterize the angiosperms as a whole.     

The great American biotic interchange and diversification history in Dynastes beetles (Scarabaeidae; Dynastinae)

Biotic interchange between geographic regions can promote rapid diversification. However, what are the important factors that determine the rate of diversification (e.g., trait‐dependent diversification) vary between study systems. The evolutionary history of Dynastes beetles, which can be found in both North and South Americas and exhibit two different altitudinal preferences (highland and lowland) is tested for the effects of biotic interchange between continents and different ecological preferences on the rate of species diversification. Additionally, the hypotheses of geological time‐dependent and lineage specific diversification rates are also tested. Results from this study indicate that in Dynastes beetles a pre‐landbridge dispersal hypothesis from South to North America is preferred and that the speciation rates estimated using BAMM are similar between lineages of different geographic origins and different altitudinal preferences (i.e., diversification rate is not trait‐dependent). On the other hand, my result from marcoevolutionary cohort analysis based on BAMM outputs suggests that the rate of speciation in Dynastes beetles is, instead of trait‐dependent (geographic and ecological), lineage specific. Furthermore, a steadily increasing speciation rate can be found in Pliocene and Pleistocene, which implies that geological and climatic events, i.e., colonizing North America, habitat reformation in the Amazonia, and forest contraction in Pleistocene, may have together shaped the current biodiversity pattern in Dynastes beetles.     

Comparing the rates of speciation and extinction between phylogenetic trees

Over the past decade or so it has become increasingly popular to use reconstructed evolutionary trees to investigate questions about the rates of speciation and extinction. Although the methodology of this field has grown substantially in its sophistication in recent years, here I will take a step back to present a very simple model that is designed to investigate the relatively straightforward question of whether the tempo of diversification (speciation and extinction) differs between two or more phylogenetic trees, without attempting to attribute a causal basis to this difference. It is a likelihood method, and I demonstrate that it generally shows type I error that is close to the nominal level. I also demonstrate that parameter estimates obtained with this approach are largely unbiased. As this method can be used to compare trees of unknown relationship, it will be particularly well‐suited to problems in which a difference in diversification rate between clades is suspected, but in which these clades are not particularly closely related. As diversification methods can easily take into account an incomplete sampling fraction, but missing lineages are assumed to be missing at random, this method is also appropriate for cases in which we have hypothesized a difference in the process of diversification between two or more focal clades, but in which many unsampled groups separate the few of interest. The method of this study is by no means an attempt to replace more sophisticated models in which, for instance, diversification depends on the state of an observed or unobserved discrete or continuous trait. Rather, my intention is to provide a complementary approach for circumstances in which a simpler hypothesis is warranted and of biological interest.     

Estimating diversification rates from phylogenetic information

Patterns of species richness reflect the balance between speciation and extinction over the evolutionary history of life. These processes are influenced by the size and geographical complexity of regions, conditions of the environment, and attributes of individuals and species. Diversity within clades also depends on age and thus the time available for accumulating species. Estimating rates of diversification is key to understanding how these factors have shaped patterns of species richness. Several approaches to calculating both relative and absolute rates of speciation and extinction within clades are based on phylogenetic reconstructions of evolutionary relationships. As the size and quality of phylogenies increases, these approaches will find broader application. However, phylogeny reconstruction fosters a perceptual bias of continual increase in species richness, and the analysis of primarily large clades produces a data selection bias. Recognizing these biases will encourage the development of more realistic models of diversification and the regulation of species richness.     

Rapid allopatric speciation in logperch darters (Percidae: Percina)

Theory predicts that clades diversifying via sympatric speciation will exhibit high diversification rates. However, the expected rate of diversification in clades characterized by allopatric speciation is less clear. Previous studies have documented significantly higher speciation rates in freshwater fish clades diversifying via sympatric versus allopatric modes, leading to suggestions that the geographic pattern of speciation can be inferred solely from knowledge of the diversification rate. We tested this prediction using an example from darters, a clade of approximately 200 species of freshwater fishes endemic to eastern North America. A resolved phylogeny was generated using mitochondrial DNA gene sequences for logperches, a monophyletic group of darters composed of 10 recognized species. Divergence times among logperch species were estimated using a fossil calibrated molecular clock in centrarchid fishes, and diversification rates in logperches were estimated using several methods. Speciation events in logperches are recent, extending from 4.20 +/- 1.06 million years ago (mya) to 0.42 +/- 0.22 mya, with most speciation events occurring in the Pleistocene. Diversification rates are high in logperches, at some nodes exceeding rates reported for well-studied adaptive radiations such as Hawaiian silverswords. The geographic pattern of speciation in logperches was investigated by examining the relationship between degree of sympatry and the absolute age of the contrast, with the result that diversification in logperches appears allopatric. The very high diversification rate observed in the logperch phylogeny is more similar to freshwater fish clades thought to represent examples of sympatric speciation than to clades representing allopatric speciation. These results demonstrate that the geographic mode of speciation for a clade cannot be inferred from the diversification rate. The empirical observation of high diversification rates in logperches demonstrates that allopatric speciation can occur rapidly.     

Diversification rates are more strongly related to microhabitat than climate in squamate reptiles (lizards and snakes)

Patterns of species richness among clades can be directly explained by the ages of clades or their rates of diversification. The factors that most strongly influence diversification rates remain highly uncertain, since most studies typically consider only a single predictor variable. Here, we explore the relative impacts of macroclimate (i.e., occurring in tropical vs. temperate regions) and microhabitat use (i.e., terrestrial, fossorial, arboreal, aquatic) on diversification rates of squamate reptile clades (lizards and snakes). We obtained data on microhabitat, macroclimatic distribution, and phylogeny for >4000 species. We estimated diversification rates of squamate clades (mostly families) from a time‐calibrated tree, and used phylogenetic methods to test relationships between diversification rates and microhabitat and macroclimate. Across 72 squamate clades, the best‐fitting model included microhabitat but not climatic distribution. Microhabitat explained ～37% of the variation in diversification rates among clades, with a generally positive impact of arboreal microhabitat use on diversification, and negative impacts of fossorial and aquatic microhabitat use. Overall, our results show that the impacts of microhabitat on diversification rates can be more important than those of climate, despite much greater emphasis on climate in previous studies.     

High speciation rate at temperate latitudes explains unusual diversity gradients in a clade of ectomycorrhizal fungi

Understanding the patterns of biodiversity through time and space is a challenging task. However, phylogeny‐based macroevolutionary models allow us to account and measure many of the processes responsible for diversity buildup, namely speciation and extinction. The general latitudinal diversity gradient (LDG) is a well‐recognized pattern describing a decline in species richness from the equator polewards. Recent macroecological studies in ectomycorrhizal (EM) fungi have shown that their LDG is shifted, peaking at temperate rather than tropical latitudes. Here we investigate this phenomenon from a macroevolutionary perspective, focusing on a well‐sampled group of edible EM mushrooms from the genus Amanita—the Caesar's mushrooms, which follow similar diversity patterns. Our approach consisted in applying a suite of models including (1) nontrait‐dependent time‐varying diversification (Bayesian analysis of macroevolutionary mixtures [BAMM]), (2) continuous trait‐dependent diversification (quantitative‐state speciation and extinction [QuaSSE]), and (3) diversity‐dependent diversification. In short, results give strong support for high speciation rates at temperate latitudes (BAMM and QuaSSE). We also find some evidence for different diversity‐dependence thresholds in “temperate” and “tropical” subclades, and little differences in diversity due to extinction. We conclude that our analyses on the Caesar's mushrooms give further evidence of a temperate‐peaking LDG in EM fungi, highlighting the importance and the implications of macroevolutionary processes in explaining diversity gradients in microorganisms.     

Terrestrialization, miniaturization and rates of diversification in African puddle frogs (Anura: Phrynobatrachidae)

Terrestrialization, the evolution of non-aquatic oviposition, and miniaturization, the evolution of tiny adult body size, are recurring trends in amphibian evolution, but the relationships among the traits that characterize these phenomena are not well understood. Furthermore, these traits have been identified as possible "key innovations" that are predicted to increase rates of speciation in those lineages in which they evolve. We examine terrestrialization and miniaturization in sub-Saharan puddle frogs (Phrynobatrachidae) in a phylogenetic context to investigate the relationship between adaptation and diversification through time. We use relative dating techniques to ascertain if character trait shifts are associated with increased diversification rates, and we evaluate the likelihood that a single temporal event can explain the evolution of those traits. Results indicate alternate reproductive modes evolved independently in Phrynobatrachus at least seven times, including terrestrial deposition of eggs and terrestrial, non-feeding larvae. These shifts towards alternate reproductive modes are not linked to a common temporal event. Contrary to the "key innovations" hypothesis, clades that exhibit alternate reproductive modes have lower diversification rates than those that deposit eggs aquatically. Adult habitat, pedal webbing and body size have no effect on diversification rates. Though these traits putatively identified as key innovations for Phrynobatrachus do not seem to be associated with increased speciation rates, they may still provide opportunities to extend into new niches, thus increasing overall diversity.     

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.     

Can extinction rates be estimated without fossils?

There is considerable interest in the possibility of using molecular phylogenies to estimate extinction rates. The present study aims at assessing the statistical performance of the birth-death model fitting approach to estimate speciation and extinction rates by comparison to the approach considering fossil data. A simulation-based approach was used. The diversification of a large number of lineages was simulated under a wide range of speciation and extinction rate values. The estimators obtained with fossils performed better than those without fossils. In the absence of fossils (e.g. with a molecular phylogeny), the speciation rate was correctly estimated in a wide range of situations; the bias of the corresponding estimator was close to zero for the largest trees. However, this estimator was substantially biased when the simulated extinction rate was high. On the other hand the estimator of extinction rate was biased in a wide range of situations. Surprisingly, this bias was lesser with medium-sized trees. Some recommendations for interpreting results from a diversification analysis are given.     

Diversity Dynamics in Nymphalidae Butterflies: Effect of Phylogenetic Uncertainty on Diversification Rate Shift Estimates

The species rich butterfly family Nymphalidae has been used to study evolutionary interactions between plants and insects. Theories of insect-hostplant dynamics predict accelerated diversification due to key innovations. In evolutionary biology, analysis of maximum credibility trees in the software MEDUSA (modelling evolutionary diversity using stepwise AIC) is a popular method for estimation of shifts in diversification rates. We investigated whether phylogenetic uncertainty can produce different results by extending the method across a random sample of trees from the posterior distribution of a Bayesian run. Using the MultiMEDUSA approach, we found that phylogenetic uncertainty greatly affects diversification rate estimates. Different trees produced diversification rates ranging from high values to almost zero for the same clade, and both significant rate increase and decrease in some clades. Only four out of 18 significant shifts found on the maximum clade credibility tree were consistent across most of the sampled trees. Among these, we found accelerated diversification for Ithomiini butterflies. We used the binary speciation and extinction model (BiSSE) and found that a hostplant shift to Solanaceae is correlated with increased net diversification rates in Ithomiini, congruent with the diffuse cospeciation hypothesis. Our results show that taking phylogenetic uncertainty into account when estimating net diversification rate shifts is of great importance, as very different results can be obtained when using the maximum clade credibility tree and other trees from the posterior distribution.     

Recent diversification rates in North American tiger beetles estimated from a dated mtDNA phylogenetic tree

Species-level phylogenies derived from DNA sequence data provide a tool for estimating diversification rates and how these rates change over time, but to date there have been few empirical studies, particularly on insect groups. We use a densely sampled phylogenetic tree based on mitochondrial DNA to investigate diversification rates in the North American tiger beetles (genus Cicindela). Using node ages estimated from sequence data and calibrated by biogeographical evidence, we estimate an average per-lineage diversification rate of at least 0.22 +/- 0.08 species/Myr over the time interval since the most recent colonization that led to a radiation within the continent. In addition, we find evidence for a weak, recent increase in the net diversification rate. This is more consistent with a late Pleistocene increase in the speciation rate than with a constant rate of background extinction, but the results are sensitive to the dating method and taxon sampling. We discuss practical limitations to phylogenetic studies of diversification rates.     

Diet and Diversification in the Evolution of Coral Reef Fishes

The disparity in species richness among evolutionary lineages is one of the oldest and most intriguing issues in evolutionary biology. Although geographical factors have been traditionally thought to promote speciation, recent studies have underscored the importance of ecological interactions as one of the main drivers of diversification. Here, we test if differences in species richness of closely related lineages match predictions based on the concept of density-dependent diversification. As radiation progresses, ecological niche-space would become increasingly saturated, resulting in fewer opportunities for speciation. To assess this hypothesis, we tested whether reef fish niche shifts toward usage of low-quality food resources (i.e. relatively low energy/protein per unit mass), such as algae, detritus, sponges and corals are accompanied by rapid net diversification. Using available molecular information, we reconstructed phylogenies of four major reef fish clades (Acanthuroidei, Chaetodontidae, Labridae and Pomacentridae) to estimate the timing of radiations of their subclades. We found that the evolution of species-rich clades was associated with a switch to low quality food in three of the four clades analyzed, which is consistent with a density-dependent model of diversification. We suggest that ecological opportunity may play an important role in understanding the diversification of reef-fish lineages.     

FiSSE: A simple nonparametric test for the effects of a binary character on lineage diversification rates

It is widely assumed that phenotypic traits can influence rates of speciation and extinction, and several statistical approaches have been used to test for correlations between character states and lineage diversification. Recent work suggests that model‐based tests of state‐dependent speciation and extinction are sensitive to model inadequacy and phylogenetic pseudoreplication. We describe a simple nonparametric statistical test (“FiSSE”) to assess the effects of a binary character on lineage diversification rates. The method involves computing a test statistic that compares the distributions of branch lengths for lineages with and without a character state of interest. The value of the test statistic is compared to a null distribution generated by simulating character histories on the observed phylogeny. Our tests show that FiSSE can reliably infer trait‐dependent speciation on phylogenies of several hundred tips. The method has low power to detect trait‐dependent extinction but can infer state‐dependent differences in speciation even when net diversification rates are constant. We assemble a range of macroevolutionary scenarios that are problematic for likelihood‐based methods, and we find that FiSSE does not show similarly elevated false positive rates. We suggest that nonparametric statistical approaches, such as FiSSE, provide an important complement to formal process‐based models for trait‐dependent diversification.     

Detecting shifts in diversification rates without fossils

Studies of shifts in diversification rates and adaptive radiations are difficult when there are no fossils because past events cannot be inferred. The phylogenies of recent species, however, allow one to infer the patterns of past diversifications. I present a new method for estimating the diversification rate of a lineage, provided that a phylogeny of recent species, constructed, for instance, with molecular data, is available. This method was inspired by survival models and takes into account species that are not included in detailed phylogenetic data, provided that approximate dates of origin of these species are known. Likelihood ratio tests and Akaike Information Criterion make it possible to test for differences in diversification among lineages or groups of lineages and, thus, to evaluate adaptive radiation hypotheses. The present modeling approach can easily be extended to include temporal variations in diversification rates. A simulation study showed that the method is statistically consistent, avoiding Type I and Type II errors, and that it is robust to periodic or random fluctuations in the speciation rate. An example is presented with a composite phylogeny of primates.