Heterogeneity in the rate of molecular sequence evolution substantially impacts the accuracy of detecting shifts in diversification rates

As species richness varies along the tree of life, there is a great interest in identifying factors that affect the rates by which lineages speciate or go extinct. To this end, theoretical biologists have developed a suite of phylogenetic comparative methods that aim to identify where shifts in diversification rates had occurred along a phylogeny and whether they are associated with some traits. Using these methods, numerous studies have predicted that speciation and extinction rates vary across the tree of life. In this study, we show that asymmetric rates of sequence evolution lead to systematic biases in the inferred phylogeny, which in turn lead to erroneous inferences regarding lineage diversification patterns. The results demonstrate that as the asymmetry in sequence evolution rates increases, so does the tendency to select more complicated models that include the possibility of diversification rate shifts. These results thus suggest that any inference regarding shifts in diversification pattern should be treated with great caution, at least until any biases regarding the molecular substitution rate have been ruled out.     

The latitudinal gradient in dispersal constraints: ecological specialisation drives diversification in tropical birds

Physiological and behavioural constraints arising from ecological specialisation are proposed to limit gene flow and promote diversification in tropical lineages. In this study, we use phylogenetic analyses to test this idea in 739 Amazonian bird species. We show that patterns of species and subspecies richness are best predicted by a suite of avian specialisms common in tropical avifaunas but rare in the temperate zone. However, this only applied to niche traits associated with dispersal limitation rather than vagility. These findings are consistent with the view that diversity is promoted by more finely partitioned niches, although not simply by coevolutionary adaptation and niche packing as is often assumed. Instead, they suggest that diversification is driven by dispersal constraints, and that niches characterised by these constraints are biased towards tropical systems. We conclude that specialised tropical niches reduce the likelihood of dispersal across barriers, thereby increasing allopatric diversification and contributing to the latitudinal diversity gradient.     

The phylogenetic signal of diversification rates

Hypotheses to explain the causes of diversity gradients have increasingly focused on the factors that actually change species numbers, namely speciation, extinction and dispersal. A common assumption of many of these hypotheses is that there should be phylogenetic signal in diversification rates, yet this assumption has rarely been tested explicitly. In this study, we compile a large data set including 328,219 species of plants, mammals, amphibians and squamates to assess the level of phylogenetic signal in their diversification rates. Significant phylogenetic signal was detected in all data sets, except for squamates, suggesting not only that closely related clades indeed might share similar diversification rates, but also that the level of phylogenetic signal might vary considerably between them. Moreover, there were intriguing differences among taxa in the rate of decay in phylogenetic autocorrelation over time, underscoring the existence of taxon-specific patterns of phylogenetic autocorrelation. These results have important implications for the development of more realistic models of species diversification.     

Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions

Diversification rate is one of the most important metrics in macroecological and macroevolutionary studies. Here I demonstrate that diversification analyses can be misleading when researchers assume that diversity increases unbounded through time, as is typical in molecular phylogenetic studies. If clade diversity is regulated by ecological factors, then species richness may be independent of clade age and it may not be possible to infer the rate at which diversity arose. This has substantial consequences for the interpretation of many studies that have contrasted rates of diversification among clades and regions. Often, it is possible to estimate the total diversification experienced by a clade but not diversification rate itself. I show that the evidence for ecological limits on diversity in higher taxa is widespread. Finally, I explore the implications of ecological limits for a variety of ecological and evolutionary questions that involve inferences about speciation and extinction rates from phylogenetic data.     

Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species

A key question in predicting responses to anthropogenic climate change is: how quickly can species adapt to different climatic conditions? Here, we take a phylogenetic approach to this question. We use 17 time‐calibrated phylogenies representing the major tetrapod clades (amphibians, birds, crocodilians, mammals, squamates, turtles) and climatic data from distributions of > 500 extant species. We estimate rates of change based on differences in climatic variables between sister species and estimated times of their splitting. We compare these rates to predicted rates of climate change from 2000 to 2100. Our results are striking: matching projected changes for 2100 would require rates of niche evolution that are > 10 000 times faster than rates typically observed among species, for most variables and clades. Despite many caveats, our results suggest that adaptation to projected changes in the next 100 years would require rates that are largely unprecedented based on observed rates among vertebrate species.     

Latitude, elevational climatic zonation and speciation in New World vertebrates

Many biodiversity hotspots are located in montane regions, especially in the tropics. A possible explanation for this pattern is that the narrow thermal tolerances of tropical species and greater climatic stratification of tropical mountains create more opportunities for climate-associated parapatric or allopatric speciation in the tropics relative to the temperate zone. However, it is unclear whether a general relationship exists among latitude, climatic zonation and the ecology of speciation. Recent taxon-specific studies obtained different results regarding the role of climate in speciation in tropical versus temperate areas. Here, we quantify overlap in the climatic distributions of 93 pairs of sister species of mammals, birds, amphibians and reptiles restricted to either the New World tropics or to the Northern temperate zone. We show that elevational ranges of tropical- and temperate-zone species do not differ from one another, yet the temperature range experienced by species in the temperate zone is greater than for those in the tropics. Moreover, tropical sister species tend to exhibit greater similarity in their climatic distributions than temperate sister species. This pattern suggests that evolutionary conservatism in the thermal niches of tropical taxa, coupled with the greater thermal zonation of tropical mountains, may result in increased opportunities for allopatric isolation, speciation and the accumulation of species in tropical montane regions. Our study exemplifies the power of combining phylogenetic and spatial datasets of global climatic variation to explore evolutionary (rather than purely ecological) explanations for the high biodiversity of tropical montane regions.     

Niche divergence and lineage diversification among closely related Sistrurus rattlesnakes

Comparing niche divergence among closely related taxa can yield important insights into the ecological distinctiveness of genetically similar forms, and identify the processes that are responsible for diversification in such organisms. Here, we apply newly developed techniques for analysing niche divergence to assess how ecologically distinct a group of closely related rattlesnakes (Sistrurus sp.) are and to explore the role that niche divergence may have played in their diversification. We find that all taxa even the most recently evolved subspecies (approximately 100,000 years old) are now ecologically distinct, implying a role for ecology in the diversification process. Statistical analysis based on comparisons with null models show that niche divergence between forms is more common than niche conservation. Finally, there is nonlinear relationship between phylogenetic and niche divergence in this group whereby niche divergence develops more rapidly between recently diverged subspecies than more distantly related forms. Overall, our results argue that ecology may play an important role in the diversification process in these snakes.     

Connectivity and vagility determine spatial richness gradients and diversification of freshwater fish in North America and Europe

The latitudinal species richness gradient (LRG) has been the subject of intense interest and many hypotheses but much less consideration has been given to longitudinal richness differences. The effect of postglacial dispersal, determined by connectivity and vagility, on richness was evaluated for the species‐poor European and North American Pacific and species‐rich Atlantic regional freshwater fish faunas. The numbers of species, by habitat, migration and distributional range categories, were determined from regional species lists for these three realms. The current orientation and past connections of drainage channels indicate that connectivity is greatest in the Atlantic and least in the Pacific. With increasing connectivity across realms, endemism decreased and postglacial recolonization increased, as did the LRG slope, with the greatest richness difference occurring between southern Atlantic and Pacific regions. Recolonizing species tended to be migratory, habitat generalists and from families of marine origin. Diversification, as indicated by species/genus ratios, probability of diversification, taxonomic distinctness and endemicity, declined with increasing latitude in all realms and was least in Europe. Richness patterns are consistent with an LRG driven by the time available for postglacial recolonization and by differences in dispersal ability, with richness differences across realms reflecting differences in dispersal and diversification.     

Asymmetries in phylogenetic diversification and character change can be untangled

The analysis of diversification and character evolution using phylogenetic data attracts increasing interest from biologists. Recent statistical developments have resulted in a variety of tools for the inference of macroevolutionary processes in a phylogenetic context. In a recent paper Maddison (2006 Evolution, 60: 1743-1746) pointed out that uncareful use of some of these tools could lead to misleading conclusions on diversification or character evolution, and thus to difficulties in distinguishing both phenomena. I here present guidelines for the analyses of macroevolutionary data that may help to avoid these problems. The proper use of recently developed statistical methods may help to untangle diversification and character change, and so will allow us to address important evolutionary questions.     

Confounding asymmetries in evolutionary diversification and character change

Studies of character evolution often assume that a phylogeny's shape is determined independently of the characters, which then evolve as mere passengers along the tree's branches. However, if the characters help shape the tree, but this is not considered, biased inferences can result. Simulations of asymmetrical speciation (i.e., one character state conferring a higher rate of speciation than another) result in data that are interpreted to show a higher rate of change toward the diversification-enhancing state, even though the rates to and from this state were in fact equal. Conversely, simulations of asymmetrical character change yield data that could be misinterpreted as showing asymmetrical rates of speciation. Studies of biased diversification and biased character change need to be unified by joint models and estimation methods, although how successfully the two processes can be teased apart remains to be seen.     

Likelihood methods for detecting temporal shifts in diversification rates

Maximum likelihood is a potentially powerful approach for investigating the tempo of diversification using molecular phylogenetic data. Likelihood methods distinguish between rate-constant and rate-variable models of diversification by fitting birth-death models to phylogenetic data. Because model selection in this context is a test of the null hypothesis that diversification rates have been constant over time, strategies for selecting best-fit models must minimize Type I error rates while retaining power to detect rate variation when it is present. Here I examine model selection, parameter estimation, and power to reject the null hypothesis using likelihood models based on the birth-death process. The Akaike information criterion (AIC) has often been used to select among diversification models; however, I find that selecting models based on the lowest AIC score leads to a dramatic inflation of the Type I error rate. When appropriately corrected to reduce Type I error rates, the birth-death likelihood approach performs as well or better than the widely used gamma statistic, at least when diversification rates have shifted abruptly over time. Analyses of datasets simulated under a range of rate-variable diversification scenarios indicate that the birth-death likelihood method has much greater power to detect variation in diversification rates when extinction is present. Furthermore, this method appears to be the only approach available that can distinguish between a temporal increase in diversification rates and a rate-constant model with nonzero extinction. I illustrate use of the method by analyzing a published phylogeny for Australian agamid lizards.     

Can the tropical conservatism hypothesis explain temperate species richness patterns? An inverse latitudinal biodiversity gradient in the New World snake tribe Lampropeltini

Aim  A latitudinal gradient in species richness, defined as a decrease in biodiversity away from the equator, is one of the oldest known patterns in ecology and evolutionary biology. However, there are also many known cases of increasing poleward diversity, forming inverse latitudinal biodiversity gradients. As only three processes (speciation, extinction and dispersal) can directly affect species richness in areas, similar factors may be responsible for both classical (high tropical diversity) and inverse (high temperate diversity) gradients. Thus, a modified explanation for differential species richness which accounts for both patterns would be preferable to one which only explains high tropical biodiversity.
Location  The New World.
Methods  We test several proposed ecological, temporal, evolutionary and spatial explanations for latitudinal diversity gradients in the New World snake tribe Lampropeltini, which exhibits its highest biodiversity in temperate regions.
Results  We find that an extratropical peak in species richness is not explained by latitudinal variation in diversification rate, the mid-domain effect, or Rapoport's rule. Rather, earlier colonization and longer duration in the temperate zones allowing more time for speciation to increase biodiversity, phylogenetic niche conservatism limiting tropical dispersal and the expansion of the temperate zones in the Tertiary better explain inverse diversity gradients in this group.
Main conclusions  Our conclusions are the inverse of the predictions made by the tropical conservatism hypothesis to explain higher biodiversity near the equator. Therefore, we suggest that the processes invoked are not intrinsic to the tropics but are dependent on historical biogeography to determine the distribution of species richness, which we refer to as the 'biogeographical conservatism hypothesis'.     

Shift in diversification in sister-clade comparisons: a more powerful test

Tests of shift in diversification associated with key innovations or directional environmental change can be performed with sister-clade comparisons. This approach is attractive because it does not require detailed phylogenetic information. I propose a new likelihood ratio test based on fitting two models of diversification. I show how this test differs from a previous likelihood ratio test based on the geometric distribution. With simulations from a wide range of situations, I show that the new test performs much better than this test and the traditional test by Slowinski and Guyer. The proposed test performs at least as well as the species richness contrast test that has been proposed by several authors in four versions. A power analysis with low number of pairs of sister clades showed that the new test could detect a shift in diversification with five or less pairs of sister clades, whereas the diversity contrast test cannot detect any shift in this situation. The former appears as more powerful than the latter, and therefore is recommended when the number of pairs of sister clades is low (less than 10). All other tests should not be used as the present study showed they lack statistical power and robustness.     

Statistical analysis of diversification with species traits

Testing whether some species traits have a significant effect on diversification rates is central in the assessment of macroevolutionary theories. However, we still lack a powerful method to tackle this objective. I present a new method for the statistical analysis of diversification with species traits. The required data are observations of the traits on recent species, the phylogenetic tree of these species, and reconstructions of ancestral values of the traits. Several traits, either continuous or discrete, and in some cases their interactions, can be analyzed simultaneously. The parameters are estimated by the method of maximum likelihood. The statistical significance of the effects in a model can be tested with likelihood ratio tests. A simulation study showed that past random extinction events do not affect the Type I error rate of the tests, whereas statistical power is decreased, though some power is still kept if the effect of the simulated trait on speciation is strong. The use of the method is illustrated by the analysis of published data on primates. The analysis of these data showed that the apparent overall positive relationship between body mass and species diversity is actually an artifact due to a clade-specific effect. Within each clade the effect of body mass on speciation rate was in fact negative. The present method allows to take both effects (clade and body mass) into account simultaneously.     

Evolution of niche width and adaptive diversification

Theoretical models suggest that resource competition can lead to the adaptive splitting of consumer populations into diverging lineages, that is, to adaptive diversification. In general, diversification is likely if consumers use only a narrow range of resources and thus have a small niche width. Here we use analytical and numerical methods to study the consequences for diversification if the niche width itself evolves. We found that the evolutionary outcome depends on the inherent costs or benefits of widening the niche. If widening the niche did not have costs in terms of overall resource uptake, then the consumer evolved a niche that was wide enough for disruptive selection on the niche position to vanish; adaptive diversification was no longer observed. However, if widening the niche was costly, then the niche widths remained relatively narrow, allowing for adaptive diversification in niche position. Adaptive diversification and speciation resulting from competition for a broadly distributed resource is thus likely if the niche width is fixed and relatively narrow or free to evolve but subject to costs. These results refine the conditions for adaptive diversification due to competition and formulate them in a way that might be more amenable for experimental investigations.     

Evolutionary diversification of reef corals: a comparison of the molecular and fossil records

Understanding historical patterns of diversity dynamics is of paramount importance for many evolutionary questions. The fossil record has long been the only source of information on patterns of diversification, but the molecular record, derived from time-calibrated phylogenies, is becoming an important additional resource. Both fossil and molecular approaches have shortcomings and biases. These have been well studied for fossil data but much less so for molecular data and empirical comparisons between approaches are lacking. Here, we compare the patterns of diversification derived from fossil and molecular data in scleractinian reef coral species. We also assess the robustness of molecular diversification rates to poor taxon sampling. We find that the temporal pattern of molecular diversification rates is robust to incomplete sampling when rates are calculated per interval. The major obstacle of molecular methods is that rate estimates are distorted because diversification rates can never be negative, whereas the fossil record suffers from incomplete preservation and inconsistent taxonomy. Nevertheless, the molecular pattern of diversification is comparable to the pattern we observe in the fossil record, with the timing of major diversification pulses coinciding in each dataset. For example, both agree that the end-Triassic coral extinction was a catastrophic bottleneck in scleractinian evolution.     

Niche width predicts extinction from climate change and vulnerability of tropical species

Climate change may be a major threat to global biodiversity, especially to tropical species. Yet, why tropical species are more vulnerable to climate change remains unclear. Tropical species are thought to have narrower physiological tolerances to temperature, and they have already experienced a higher estimated frequency of climate-related local extinctions. These two patterns suggest that tropical species are more vulnerable to climate change because they have narrower thermal niche widths. However, no studies have tested whether species with narrower climatic niche widths for temperature have experienced more local extinctions, and if these narrower niche widths can explain the higher frequency of tropical local extinctions. Here, we test these ideas using resurvey data from 538 plant and animal species from 10 studies. We found that mean niche widths among species and the extent of climate change (increase in maximum annual temperatures) together explained most variation (>75%) in the frequency of local extinction among studies. Surprisingly, neither latitude nor occurrence in the tropics alone significantly predicted local extinction among studies, but latitude and niche widths were strongly inversely related. Niche width also significantly predicted local extinction among species, as well as among and (sometimes) within studies. Overall, niche width may offer a relatively simple and accessible predictor of the vulnerability of populations to climate change. Intriguingly, niche width has the best predictive power to explain extinction from global warming when it incorporates coldest yearly temperatures.     

Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis

Gasteroid fungi include puffballs, stinkhorns, and other forms that produce their spores inside the fruiting body. Gasteroid taxa comprise about 8.4% of the Agaricomycetes (mushroom-forming fungi) and have evolved numerous times from nongasteroid ancestors, such as gilled mushrooms, polypores, and coral fungi, which produce spores on the surface of the fruiting body. Nongasteroid Agaricomycetes have a complex mechanism of forcible spore discharge that is lost in gasteroid lineages, making reversals to nongasteroid forms very unlikely. Our objective was to determine whether gasteromycetation affects the rate of diversification of lineages "trapped" in the gasteroid state. We assembled four datasets (the Sclerodermatineae, Boletales, Phallomycetidae, and Lycoperdaceae), representing unique origins of gasteroid fungi from nongasteroid ancestors and generated phylogenies using BEAST. Using the program Diversitree, we analyzed these phylogenies to estimate character-state-specific rates of speciation and extinction, and rates of transitions between nongasteroid and gasteroid forms. Most optimal models suggest that the net diversification rate of gasteroid forms exceeds that of nongasteroid forms, and that gasteroid forms will eventually come to predominate over nongasteroid forms in the clades in which they have arisen. The low frequency of gasteroid forms in the Agaricomycetes as a whole may reflect the recent origins of many gasteroid lineages.