EXPLOSIVE EVOLUTIONARY RADIATIONS: DECREASING SPECIATION OR INCREASING EXTINCTION THROUGH TIME?

A common pattern in time-calibrated molecular phylogenies is a signal of rapid diversification early in the history of a radiation. Because the net rate of diversification is the difference between speciation and extinction rates, such "explosive-early" diversification could result either from temporally declining speciation rates or from increasing extinction rates through time. Distinguishing between these alternatives is challenging but important, because these processes likely result from different ecological drivers of diversification. Here we develop a method for estimating speciation and extinction rates that vary continuously through time. By applying this approach to real phylogenies with explosive-early diversification and by modeling features of lineage-accumulation curves under both declining speciation and increasing extinction scenarios, we show that a signal of explosive-early diversification in phylogenies of extant taxa cannot result from increasing extinction and can only be explained by temporally declining speciation rates. Moreover, whenever extinction rates are high, "explosive early" patterns become unobservable, because high extinction quickly erases the signature of even large declines in speciation rates. Although extinction may obscure patterns of evolutionary diversification, these results show that decreasing speciation is often distinguishable from increasing extinction in the numerous molecular phylogenies of radiations that retain a preponderance of early lineages.     

Investigating the timing of origin and evolutionary processes shaping regional species diversity: Insights from simulated data and neotropical butterfly diversification rates

Different diversification scenarios have been proposed to explain the origin of extant biodiversity. However, most existing meta‐analyses of time‐calibrated phylogenies rely on approaches that do not quantitatively test alternative diversification processes. Here, I highlight the shortcomings of using species divergence ranks, which is a method widely used in meta‐analyses. Divergence ranks consist of categorizing cladogenetic events to certain periods of time, typically to either Pleistocene or to pre‐Pleistocene ages. This approach has been claimed to shed light on the origin of most extant species and the timing and dynamics of diversification in any biogeographical region. However, interpretations drawn from such method often confound two fundamental questions in macroevolutionary studies, tempo (timing of evolutionary rate shifts) and mode (“how” and “why” of speciation). By using simulated phylogenies under four diversification scenarios, constant‐rate, diversity‐dependence, high extinction, and high speciation rates in the Pleistocene, I showed that interpretations based on species divergence ranks might have been seriously misleading. Future meta‐analyses of dated phylogenies need to be aware of the impacts of incomplete taxonomic sampling, tree topology, and divergence time uncertainties, as well as they might be benefited by including quantitative tests of alternative diversification models that acknowledge extinction and diversity dependence.     

ESTIMATING THE DURATION OF SPECIATION FROM PHYLOGENIES

Speciation is not instantaneous but takes time. The protracted birth–death diversification model incorporates this fact and predicts the often observed slowdown of lineage accumulation toward the present. The mathematical complexity of the protracted speciation model has barred estimation of its parameters until recently a method to compute the likelihood of phylogenetic branching times under this model was outlined (Lambert et al. 2014 ). Here, we implement this method and study using simulated phylogenies of extant species how well we can estimate the model parameters (rate of initiation of speciation, rate of extinction of incipient and good species, and rate of completion of speciation) as well as the duration of speciation, which is a combination of the aforementioned parameters. We illustrate our approach by applying it to a primate phylogeny. The simulations show that phylogenies often do not contain enough information to provide unbiased estimates of the speciation‐initiation rate and the extinction rate, but the duration of speciation can be estimated without much bias. The estimate of the duration of speciation for the primate clade is consistent with literature estimates. We conclude that phylogenies combined with the protracted speciation model provide a promising way to estimate the duration of speciation.     

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.     

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.     

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.     

Extinction can be estimated from moderately sized molecular phylogenies

Hundreds of studies have been dedicated to estimating speciation and extinction from phylogenies of extant species. Although it has long been known that estimates of extinction rates using trees of extant organisms are often uncertain, an influential paper by Rabosky (2010) suggested that when birth rates vary continuously across the tree, estimates of the extinction fraction (i.e., extinction rate/speciation rate) will appear strongly bimodal, with a peak suggesting no extinction and a peak implying speciation and extinction rates are approaching equality. On the basis of these results, and the realistic nature of this form of rate variation, it is now generally assumed by many practitioners that extinction cannot be understood from molecular phylogenies alone. Here, we reevaluated and extended the analyses of Rabosky (2010) and come to the opposite conclusion—namely, that it is possible to estimate extinction from molecular phylogenies, even with model violations due to heritable variation in diversification rate. Note that while it may be tempting to interpret our study as advocating the application of simple birth–death models, our goal here is to show how a particular model violation does not necessitate the abandonment of an entire field: use prudent caution, but do not abandon all hope.     

EXTINCTION DURING EVOLUTIONARY RADIATIONS: RECONCILING THE FOSSIL RECORD WITH MOLECULAR PHYLOGENIES

Recent application of time‐varying birth–death models to molecular phylogenies suggests that a decreasing diversification rate can only be observed if there was a decreasing speciation rate coupled with extremely low or no extinction. However, from a paleontological perspective, zero extinction rates during evolutionary radiations seem unlikely. Here, with a more comprehensive set of computer simulations, we show that substantial extinction can occur without erasing the signal of decreasing diversification rate in a molecular phylogeny. We also find, in agreement with the previous work, that a decrease in diversification rate cannot be observed in a molecular phylogeny with an increasing extinction rate alone. Further, we find that the ability to observe decreasing diversification rates in molecular phylogenies is controlled (in part) by the ratio of the initial speciation rate (Lambda) to the extinction rate (Mu) at equilibrium (the LiMe ratio), and not by their absolute values. Here we show in principle, how estimates of initial speciation rates may be calculated using both the fossil record and the shape of lineage through time plots derived from molecular phylogenies. This is important because the fossil record provides more reliable estimates of equilibrium extinction rates than initial speciation rates.     

Detecting shifts in diversity limits from molecular phylogenies: what can we know?

Large complete species-level molecular phylogenies can provide the most direct information about the macroevolutionary history of clades having poor fossil records. However, extinction will ultimately erode evidence of pulses of rapid speciation in the deep past. Assessment of how well, and for how long, phylogenies retain the signature of such pulses has hitherto been based on a--probably untenable--model of ongoing diversity-independent diversification. Here, we develop two new tests for changes in diversification 'rules' and evaluate their power to detect sudden increases in equilibrium diversity in clades simulated with diversity-dependent speciation and extinction rates. Pulses of diversification are only detected easily if they occurred recently and if the rate of species turnover at equilibrium is low; rates reported for fossil mammals suggest that the power to detect a doubling of species diversity falls to 50 per cent after less than 50 Myr even with a perfect phylogeny of extant species. Extinction does eventually draw a veil over past dynamics, suggesting that some questions are beyond the limits of inference, but sudden clade-wide pulses of speciation can be detected after many millions of years, even when overall diversity is constrained. Applying our methods to existing phylogenies of mammals and angiosperms identifies intervals of elevated diversification in each.     

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.     

Ephemeral ecological speciation and the latitudinal biodiversity gradient

The richness of biodiversity in the tropics compared to high‐latitude parts of the world forms one of the most globally conspicuous patterns in biology, and yet few hypotheses aim to explain this phenomenon in terms of explicit microevolutionary mechanisms of speciation and extinction. We link population genetic processes of selection and adaptation to speciation and extinction by way of their interaction with environmental factors to drive global scale macroecological patterns. High‐latitude regions are both cradle and grave with respect to species diversification. In particular, we point to a conceptual equivalence of “environmental harshness” and “hard selection” as eco‐evolutionary drivers of local adaptation and ecological speciation. By describing how ecological speciation likely occurs more readily at high latitudes, with such nascent species especially prone to extinction by fusion, we derive the ephemeral ecological speciation hypothesis as an integrative mechanistic explanation for latitudinal gradients in species turnover and the net accumulation of biodiversity.     

Bayesian estimation of speciation and extinction probabilities from (in)complete phylogenies

Speciation and extinction probabilities can be estimated from molecular phylogenies of extant species that are complete at the species level. Because only a fraction of published phylogenies is complete at the species level, methods have been developed to estimate speciation and extinction probabilities also from incomplete phylogenies. However, due to different estimation techniques, estimates from complete and incomplete phylogenies are difficult to compare statistically. Here I show with some examples how existing likelihood functions can be used to obtain Bayesian estimates of speciation and extinction probabilities, and how this approach is applied to both complete and incomplete phylogenies.     

Conceptual and statistical problems with the DEC+J model of founder‐event speciation and its comparison with DEC via model selection

Phylogenetic studies of geographic range evolution are increasingly using statistical model selection methods to choose among variants of the dispersal‐extinction‐cladogenesis (DEC) model, especially between DEC and DEC+J, a variant that emphasizes “jump dispersal,” or founder‐event speciation, as a type of cladogenetic range inheritance scenario. Unfortunately, DEC+J is a poor model of founder‐event speciation, and statistical comparisons of its likelihood with DEC are inappropriate. DEC and DEC+J share a conceptual flaw: cladogenetic events of range inheritance at ancestral nodes, unlike anagenetic events of dispersal and local extinction along branches, are not modelled as being probabilistic with respect to time. Ignoring this probability factor artificially inflates the contribution of cladogenetic events to the likelihood, and leads to underestimates of anagenetic, time‐dependent range evolution. The flaw is exacerbated in DEC+J because not only is jump dispersal allowed, expanding the set of cladogenetic events, its probability relative to non‐jump events is assigned a free parameter, j, that when maximized precludes the possibility of non‐jump events at ancestral nodes. DEC+J thus parameterizes the mode of speciation, but like DEC, it does not parameterize the rate of speciation. This inconsistency has undesirable consequences, such as a greater tendency towards degenerate inferences in which the data are explained entirely by cladogenetic events (at which point branch lengths become irrelevant, with estimated anagenetic rates of 0). Inferences with DEC+J can in some cases depart dramatically from intuition, e.g. when highly unparsimonious numbers of jump dispersal events are required solely because j is maximized. Statistical comparison with DEC is inappropriate because a higher DEC+J likelihood does not reflect a more close approximation of the “true” model of range evolution, which surely must include time‐dependent processes; instead, it is simply due to more weight being allocated (via j) to jump dispersal events whose time‐dependent probabilities are ignored. In testing hypotheses about the geographic mode of speciation, jump dispersal can and should instead be modelled using existing frameworks for state‐dependent lineage diversification in continuous time, taking appropriate cautions against Type I errors associated with such methods. For simple inference of ancestral ranges on a fixed phylogeny, a DEC‐based model may be defensible if statistical model selection is not used to justify the choice, and it is understood that inferences about cladogenetic range inheritance lack any relation to time, normally a fundamental axis of evolutionary models.     

Detecting local diversity‐dependence in diversification

Whether there are ecological limits to species diversification is a hotly debated topic. Molecular phylogenies show slowdowns in lineage accumulation, suggesting that speciation rates decline with increasing diversity. A maximum‐likelihood (ML) method to detect diversity‐dependent (DD) diversification from phylogenetic branching times exists, but it assumes that diversity‐dependence is a global phenomenon and therefore ignores that the underlying species interactions are mostly local, and not all species in the phylogeny co‐occur locally. Here, we explore whether this ML method based on the nonspatial diversity‐dependence model can detect local diversity‐dependence, by applying it to phylogenies, simulated with a spatial stochastic model of local DD speciation, extinction, and dispersal between two local communities. We find that type I errors (falsely detecting diversity‐dependence) are low, and the power to detect diversity‐dependence is high when dispersal rates are not too low. Interestingly, when dispersal is high the power to detect diversity‐dependence is even higher than in the nonspatial model. Moreover, estimates of intrinsic speciation rate, extinction rate, and ecological limit strongly depend on dispersal rate. We conclude that the nonspatial DD approach can be used to detect diversity‐dependence in clades of species that live in not too disconnected areas, but parameter estimates must be interpreted cautiously.     

Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record

The branching times of molecular phylogenies allow us to infer speciation and extinction dynamics even when fossils are absent. Troublingly, phylogenetic approaches usually return estimates of zero extinction, conflicting with fossil evidence. Phylogenies and fossils do agree, however, that there are often limits to diversity. Here, we present a general approach to evaluate the likelihood of a phylogeny under a model that accommodates diversity-dependence and extinction. We find, by likelihood maximization, that extinction is estimated most precisely if the rate of increase in the number of lineages in the phylogeny saturates towards the present or first decreases and then increases. We demonstrate the utility and limits of our approach by applying it to the phylogenies for two cases where a fossil record exists (Cetacea and Cenozoic macroperforate planktonic foraminifera) and to three radiations lacking fossil evidence (Dendroica, Plethodon and Heliconius). We propose that the diversity-dependence model with extinction be used as the standard model for macro-evolutionary dynamics because of its biological realism and flexibility.     

Challenges in the estimation of extinction from molecular phylogenies: A response to Beaulieu and O'Meara

Time‐calibrated phylogenies that contain only living species have been widely used to study the dynamics of speciation and extinction. Concerns about the reliability of phylogenetic extinction estimates were raised by Rabosky (2010), where I suggested that unaccommodated heterogeneity in speciation rate could lead to positively biased extinction estimates. In a recent article, Beaulieu and O'Meara (2015a) correctly point out several technical errors in the execution of my 2010 study and concluded that phylogenetic extinction estimates are robust to speciation rate heterogeneity under a range of model parameters. I demonstrate that Beaulieu and O'Meara underestimated the magnitude of speciation rate variation in real phylogenies and consequently did not incorporate biologically meaningful levels of rate heterogeneity into their simulations. Using parameter values drawn from the recent literature, I find that modest levels of heterogeneity in speciation rate result in a consistent, positive bias in extinction estimates that are exacerbated by phylogenetic tree size. This bias, combined with the inherent lack of information about extinction in molecular phylogenies, suggests that extinction rate estimates from phylogenies of extant taxa only should be treated with caution.     

Primate diversification inferred from phylogenies and fossils

Biodiversity arises from the balance between speciation and extinction. Fossils record the origins and disappearance of organisms, and the branching patterns of molecular phylogenies allow estimation of speciation and extinction rates, but the patterns of diversification are frequently incongruent between these two data sources. I tested two hypotheses about the diversification of primates based on ～600 fossil species and 90% complete phylogenies of living species: (1) diversification rates increased through time; (2) a significant extinction event occurred in the Oligocene. Consistent with the first hypothesis, analyses of phylogenies supported increasing speciation rates and negligible extinction rates. In contrast, fossils showed that while speciation rates increased, speciation and extinction rates tended to be nearly equal, resulting in zero net diversification. Partially supporting the second hypothesis, the fossil data recorded a clear pattern of diversity decline in the Oligocene, although diversification rates were near zero. The phylogeny supported increased extinction ～34 Ma, but also elevated extinction ～10 Ma, coinciding with diversity declines in some fossil clades. The results demonstrated that estimates of speciation and extinction ignoring fossils are insufficient to infer diversification and information on extinct lineages should be incorporated into phylogenetic analyses.     

Extinction and time help drive the marine‐terrestrial biodiversity gradient: is the ocean a deathtrap?

The marine‐terrestrial richness gradient is among Earth's most dramatic biodiversity patterns, but its causes remain poorly understood. Here, we analyse detailed phylogenies of amniote clades, paleontological data and simulations to reveal the mechanisms underlying low marine richness, emphasising speciation, extinction and colonisation. We show that differences in diversification rates (speciation minus extinction) between habitats are often weak and inconsistent with observed richness patterns. Instead, the richness gradient is explained by limited time for speciation in marine habitats, since all extant marine clades are relatively young. Paleontological data show that older marine invasions have consistently ended in extinction. Simulations show that marine extinctions help drive the pattern of young, depauperate marine clades. This role for extinction is not discernible from molecular phylogenies alone, and not predicted by most previously hypothesised explanations for this gradient. Our results have important implications for the marine‐terrestrial biodiversity gradient, and studies of biodiversity gradients in general.     

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.