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.     

Clade age and not diversification rate explains species richness among animal taxa

Animal taxa show remarkable variability in species richness across phylogenetic groups. Most explanations for this disparity postulate that taxa with more species have phenotypes or ecologies that cause higher diversification rates (i.e., higher speciation rates or lower extinction rates). Here we show that clade longevity, and not diversification rate, has primarily shaped patterns of species richness across major animal clades: more diverse taxa are older and thus have had more time to accumulate species. Diversification rates calculated from 163 species-level molecular phylogenies were highly consistent within and among three major animal phyla (Arthropoda, Chordata, Mollusca) and did not correlate with species richness. Clades with higher estimated diversification rates were younger, but species numbers increased with increasing clade age. A fossil-based data set also revealed a strong, positive relationship between total extant species richness and crown group age across the orders of insects and vertebrates. These findings do not negate the importance of ecology or phenotype in influencing diversification rates, but they do show that clade longevity is the dominant signal in major animal biodiversity patterns. Thus, some key innovations may have acted through fostering clade longevity and not by heightening diversification rate.     

Species richness among birds: body size,life history,sexual selection or ecology?

Why do some avian families contain so many more species than other families? We use comparisons between sister taxa to test predictions arising from six explanations to this puzzle: that differences between families are due to chance, body size, life history, sexual selection, intrinsic ecological factors or extrinsic abiotic factors, respectively. In agreement with previous analyses, we find no support for the idea that differences in species richness are simply due to chance. However, contrary to most previous work, we also find no support for the hypotheses that high species richness is correlated with small body size and fast life history. Rather, high species diversity is strongly associated with pronounced plumage dichromatism, generalist feeding habits and good dispersal capabilities as well as large and fragmented geographical ranges. In addition, all of these relationships are robust to the removal of the two most speciose avian lineages, the Ciconiiformes and the Passeriformes. The supposed relationships between species richness and both body size and life history are, however, due to phylogenetic non-independence. Together with previous work showing that differences between avian lineages in extinction risk are associated with variation in body size and life history, these results indicate that extinction rates and speciation rates are not necessarily determined by the same factors. Hence, high extinction rates are not inevitably associated with low speciation rates. Extinction-prone lineages may, in fact, have a high rate of speciation. In such lineages a high proportion of ''vulnerable'' species would be a natural, ongoing phenomenon.     

Global diversification rates of passerine birds

The distribution of species richness in families of passerine birds suggests that the net rate of diversification was significantly higher than average in as many as 7 out of 47 families. However, the absence of excess species richness among the 106 tribes within these families indicates that these high rates were transient, perhaps associated in some cases with tectonic movements or dispersal events that extended geographical ranges. Thus, large clade size among passerine birds need not represent intrinsic key innovations that influence the rate of diversification. Approximately 17 families and 30 tribes have too few species relative to other passerine taxa. Many of these are ecologically or geographically marginal, being especially overrepresented in the Australasian region. Observed intervals between lineage splitting suggest that extinction has occurred ca. 90% as frequently as speciation (waiting times of 1.03 and 0.93 Myr) and that the 47 modern families comprising 5712 species descended from approximately 430 passerine lineages extant 24 Myr ago. Speciation and extinction rates among small, marginal families might be 1-2 orders of magnitude lower.     

The shape and temporal dynamics of phylogenetic trees arising from geographic speciation

Phylogenetic trees often depart from the expectations of stochastic models, exhibiting imbalance in diversification among lineages and slowdowns in the rate of lineage accumulation through time. Such departures have led to a widespread perception that ecological differences among species or adaptation and subsequent niche filling are required to explain patterns of diversification. However, a key element missing from models of diversification is the geographical context of speciation and extinction. In this study, we develop a spatially explicit model of geographic range evolution and cladogenesis, where speciation arises via vicariance or peripatry, and explore the effects of these processes on patterns of diversification. We compare the results with those observed in 41 reconstructed avian trees. Our model shows that nonconstant rates of speciation and extinction are emergent properties of the apportioning of geographic ranges that accompanies speciation. The dynamics of diversification exhibit wide variation, depending on the mode of speciation, tendency for range expansion, and rate of range evolution. By varying these parameters, the model is able to capture many, but not all, of the features exhibited by birth-death trees and extant bird clades. Under scenarios with relatively stable geographic ranges, strong slowdowns in diversification rates are produced, with faster rates of range dynamics leading to constant or accelerating rates of apparent diversification. A peripatric model of speciation with stable ranges also generates highly unbalanced trees typical of bird phylogenies but fails to produce realistic range size distributions among the extant species. Results most similar to those of a birth-death process are reached under a peripatric speciation scenario with highly volatile range dynamics. Taken together, our results demonstrate that considering the geographical context of speciation and extinction provides a more conservative null model of diversification and offers a very different perspective on the phylogenetic patterns expected in the absence of ecology.     

Extinction, ecological opportunity, and the origins of global snake diversity

Snake diversity varies by at least two orders of magnitude among extant lineages, with numerous groups containing only one or two species, and several young clades exhibiting exceptional richness (>700 taxa). With a phylogeny containing all known families and subfamilies, we find that these patterns cannot be explained by background rates of speciation and extinction. The majority of diversity appears to derive from a radiation within the superfamily Colubroidea, potentially stemming from the colonization of new areas and the evolution of advanced venom-delivery systems. In contrast, negative relationships between clade age, clade size, and diversification rate suggest the potential for possible bias in estimated diversification rates, interpreted by some recent authors as support for ecologically mediated limits on diversity. However, evidence from the fossil record indicates that numerous lineages were far more diverse in the past, and that extinction has had an important impact on extant diversity patterns. Thus, failure to adequately account for extinction appears to prevent both rate- and diversity-limited models from fully characterizing richness dynamics in snakes. We suggest that clade-level extinction may provide a key mechanism for explaining negative or hump-shaped relationships between clade age and diversity, and the prevalence of ancient, species-poor lineages in numerous groups.     

Primary controls on species richness in higher taxa

The disparity in species richness across the tree of life is one of the most striking and pervasive features of biological diversity. Some groups are exceptionally diverse, whereas many other groups are species poor. Differences in diversity among groups are frequently assumed to result from primary control by differential rates of net diversification. However, a major alternative explanation is that ecological and other factors exert primary control on clade diversity, such that apparent variation in net diversification rates is a secondary consequence of ecological limits on clade growth. Here, I consider a likelihood framework for distinguishing between these competing hypotheses. I incorporate hierarchical modeling to explicitly relax assumptions about the constancy of diversification rates across clades, and I propose several statistics for a posteriori evaluation of model adequacy. I apply the framework to a recent dated phylogeny of ants. My results reject the hypothesis that net diversification rates exert primary control on species richness in this group and demonstrate that clade diversity is better explained by total time-integrated speciation. These results further suggest that it may not possible to estimate meaningful speciation and extinction rates from higher-level phylogenies of extant taxa only.     

The causes of species richness patterns across space, time, and clades and the role of "ecological limits"

A major goal of research in ecology and evolution is to explain why species richness varies across habitats, regions, and clades. Recent reviews have argued that species richness patterns among regions and clades may be explained by "ecological limits" on diversity over time, which are said to offer an alternative explanation to those invoking speciation and extinction (diversification) and time. Further, it has been proposed that this hypothesis is best supported by failure to find a positive relationship between time (e.g., clade age) and species richness. Here, I critically review the evidence for these claims, and propose how we might better study the ecological and evolutionary origins of species richness patterns. In fact, ecological limits can only influence species richness in clades by influencing speciation and extinction, and so this new "alternative paradigm" is simply one facet of the traditional idea that ecology influences diversification. The only direct evidence for strict ecological limits on richness (i.e., constant diversity over time) is from the fossil record, but many studies cited as supporting this pattern do not, and there is evidence for increasing richness over time. Negative evidence for a relationship between clade age and richness among extant clades is not positive evidence for constant diversity over time, and many recent analyses finding no age-diversity relationship were biased to reach this conclusion. More comprehensive analyses strongly support a positive age-richness relationship. There is abundant evidence that both time and ecological influences on diversification rates are important drivers of both large-scale and small-scale species richness patterns. The major challenge for future studies is to understand the ecological and evolutionary mechanisms underpinning the relationships between time, dispersal, diversification, and species richness patterns.     

THE ROLE OF CLIMATIC TOLERANCES AND SEED TRAITS IN REDUCED EXTINCTION RATES OF TEMPERATE POLYGONACEAE

The latitudinal diversity gradient (LDG) is one of the most striking and consistent biodiversity patterns across taxonomic groups. We investigate the species richness gradient in the buckwheat family, Polygonaceae, which exhibits a reverse LDG and is, thus, decoupled from dominant gradients of energy and environmental stability that increase toward the tropics and confound mechanistic interpretations. We test competing age and evolutionary diversification hypotheses, which may explain the diversification of this plant family over the past 70 million years. Our analyses show that the age hypothesis, which posits that clade richness is positively correlated with the ecological and evolutionary time since clade origin, fails to explain the richness gradient observed in Polygonaceae. However, an evolutionary diversification hypothesis is highly supported, with diversification rates being 3.5 times higher in temperate clades compared to tropical clades. We demonstrate that differences in rates of speciation, migration, and molecular evolution insufficiently explain the observed patterns of differential diversification rates. We suggest that reduced extinction rates in temperate clades may be associated with adaptive responses to selection, through which seed morphology and climatic tolerances potentially act to minimize risk in temporally variable environments. Further study is needed to understand causal pathways among these traits and factors correlated with latitude.     

Molecular phylogenies and historical biogeography of a circumtropical group of gastropods (Genus: Nerita): implications for regional diversity patterns in the marine tropics

To determine how historical processes, namely speciation, extinction, and dispersal, have contributed to regional species diversity patterns across the marine tropics, we examined the biogeographical history of a circumtropical genus of intertidal gastropods. A species-level phylogeny of Nerita, representing approximately 87% of extant species, was developed from 1608bp of mitochondrial (COI and 16S) and nuclear (ATPSalpha) markers. Phylogenetic relationships generally corresponded to prior classifications; however, comprehensive sampling revealed a number of previously undetected ESUs. Using the resulting tree as a framework, we combined geographical distributions and fossil evidence to reconstruct ancestral ranges, produce a time-calibrated chronogram, and estimate diversification rates. Analyses revealed two monophyletic eastern Pacific+Atlantic (EPA) clades, each of which likely split from an Indo-West Pacific (IWP) sister clade prior to an early Miocene Tethys Seaway closure. More recent diversification throughout the IWP appears to have been driven by both vicariance and dispersal events; EPA diversity has been further shaped by speciation across the Central American Seaway prior to its closure and dispersal across the Atlantic. Despite the latter, inter-regional dispersal has been rare, and likely contributes little to regional diversity patterns. Similarly, infrequent transitions into temperate regions combined with reduced diversification rates may explain low diversity in West and South Pacific clades. Since origination, Nerita diversification appears remarkably constant, with the exception of a lag in the late Eocene-early Oligocene and elevated rates in the late Oligocene-early Miocene. However, a comparison among regions suggested that IWP clades have experienced, on average, higher rates of speciation. Fossil evidence indicates that the EPA likely witnessed greater extinction relative to the IWP. We propose that regional differences in species diversity in Nerita have been largely shaped by differential rates of speciation and extinction.     

Evolutionary diversification of clades of squamate reptiles

We analysed the diversification of squamate reptiles (7488 species) based on a new molecular phylogeny, and compared the results to similar estimates for passerine birds (5712 species). The number of species in each of 36 squamate lineages showed no evidence of phylogenetic conservatism. Compared with a random speciation-extinction process with parameters estimated from the size distribution of clades, the alethinophidian snakes (2600 species) were larger than expected and 13 clades, each having fewer than 20 species, were smaller than expected, indicating rate heterogeneity. From a lineage-through-time plot, we estimated that a provisional rate of lineage extinction (0.66 per Myr) was 94% of the rate of lineage splitting (0.70 per Myr). Diversification in squamate lineages was independent of their stem age, but strongly related to the area of the region within which they occur. Tropical vs. temperate latitude exerted a marginally significant influence on species richness. In comparison with passerine birds, squamates share several clade features, including: (1) independence of species richness and age; (2) lack of phylogenetic signal with respect to clade size; (3) general absence of exceptionally large clades; (4) over-representation of small clades; (5) influence of region size on clade size; and (6) similar rates of speciation and extinction. The evidence for both groups suggests that clade size has achieved long-term equilibrium, suggesting negative feedback of species richness on the rate of diversification.     

Species-genus ratios reflect a global history of diversification and range expansion in marine bivalves

The distribution of marine bivalve species among genera and higher taxa takes the form of the classic hollow curve, wherein few lineages are species rich and many are species poor. The distribution of species among genera (S/G ratio) varies with latitude, with temperate S/G's falling within the null expectation, and tropical and polar S/G's exceeding it. Here, we test several hypotheses for this polar overdominance in the species richness of small numbers of genera. We find a significant positive correlation between the latitudinal range of a genus and its species richness, both globally and within regions. Genus age and species richness are also positively related, but this relationship breaks down when the analysis is limited to genera endemic to climate zones or with narrow latitudinal ranges. The data suggest a link between speciation and range-expansion, with genera expanding out of the tropical latitudinal bins tending to speciate more prolifically, both globally and regionally. These genera contain more species within climate zones than taxa endemic to that zone. Range expansion thus appears to be fundamentally coupled with speciation, producing the skewed distribution of species among genera, both globally and regionally, whereas clade longevity is achieved through extinction -- resistance conferred by broad geographical ranges.     

No evidence that sexual selection is an 'engine of speciation' in birds

Abstract Sexual selection has been implicated as having a role in promoting speciation, as it should increase the rate of evolution of reproductive isolation, and there is some comparative evidence that sexual selection may be related to imbalances in clade size seen in resolved phylogenies. By employing a new comparative method we are able to investigate the role of sexual selection in explaining the patterns of species richness across birds. We used data for testes size as an index of post‐mating sexual selection, and sexual size dimorphism and sexual dichromatism as indices of pre‐mating sexual selection. These measures were obtained for 1031 species representing 467 genera. None of the variables investigated explained the patterns of species richness. As sexual selection may also increase extinction rates, the net effect on species richness in any given clade will depend on the balancing effects of sexual selection upon speciation and extinction rates. We suggest that variance across clades in this balance may have resulted in the lack of a relationship between species richness and sexual selection seen in birds.     

Temporal Patterns of Diversification across Global Cichlid Biodiversity (Acanthomorpha: Cichlidae)

The contrasting distribution of species diversity across the major lineages of cichlids makes them an ideal group for investigating macroevolutionary processes. In this study, we investigate whether different rates of diversification may explain the disparity in species richness across cichlid lineages globally. We present the most taxonomically robust time-calibrated hypothesis of cichlid evolutionary relationships to date. We then utilize this temporal framework to investigate whether both species-rich and depauperate lineages are associated with rapid shifts in diversification rates and if exceptional species richness can be explained by clade age alone. A single significant rapid rate shift increase is detected within the evolutionary history of the African subfamily Pseudocrenilabrinae, which includes the haplochromins of the East African Great Lakes. Several lineages from the subfamilies Pseudocrenilabrinae (Australotilapiini, Oreochromini) and Cichlinae (Heroini) exhibit exceptional species richness given their clade age, a net rate of diversification, and relative rates of extinction, indicating that clade age alone is not a sufficient explanation for their increased diversity. Our results indicate that the Neotropical Cichlinae includes lineages that have not experienced a significant rapid burst in diversification when compared to certain African lineages (rift lake). Neotropical cichlids have remained comparatively understudied with regard to macroevolutionary patterns relative to African lineages, and our results indicate that of Neotropical lineages, the tribe Heroini may have an elevated rate of diversification in contrast to other Neotropical cichlids. These findings provide insight into our understanding of the diversification patterns across taxonomically disparate lineages in this diverse clade of freshwater fishes and one of the most species-rich families of vertebrates.     

Biogeographical basis of recent phenotypic divergence among birds: a global study of subspecies richness

Theory predicts that biogeographic factors should play a central role in promoting population divergence and speciation. Previous empirical studies into biogeography and diversification have been relatively restricted in terms of the geographical area, phylogenetic scope, and the range of biogeographic factors considered. Here we present a global analysis of allopatric phenotypic divergence (measured as subspecies richness) across more than 9600 bird species. The main aim of this study was to examine the extent to which biogeographical factors can explain patterns of phenotypic divergence. Analysis of the taxonomic distribution of subspecies among species suggests that subspecies formation and extinction have occurred at a considerably faster rate than has species formation. However, the observed distribution departs from the expectation under a random birth-death model of diversification. Across 19 phylogenetic trees, we find no significant linear relationship between species age and subspecies richness, implying that species age is a poor predictor of subspecies richness. Both subspecies richness and subspecies diversification rate are found to exhibit low phylogenetic signal, meaning that closely related species do not tend to possess similar numbers of subspecies. As predicted by theory, high subspecies richness was associated with large breeding range size, island dwelling, inhabitation of montane regions, habitat heterogeneity, and low latitude. Of these factors, breeding range size was the variable that explained the most variation. Unravelling whether species that have invaded previously glacial areas have more or fewer subspecies than expected proves to be complicated due to a covariation between the postglacial colonization, latitude, geographic range size, and subspecies richness. However, the effect of postglacial colonization on subspecies richness appears to be small. Mapping the distribution of species' subspecies richness globally reveals geographical patterns that correspond to many of the predictions of the statistical models, but may also reflect geographical variation in taxonomic practice. Overall, we demonstrate that biogeographic models can explain about 30% of the global variation in subspecies richness in birds.     

Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography

A latitudinal gradient in biodiversity has existed since before the time of the dinosaurs, yet how and why this gradient arose remains unresolved. Here we review two major hypotheses for the origin of the latitudinal diversity gradient. The time and area hypothesis holds that tropical climates are older and historically larger, allowing more opportunity for diversification. This hypothesis is supported by observations that temperate taxa are often younger than, and nested within, tropical taxa, and that diversity is positively correlated with the age and area of geographical regions. The diversification rate hypothesis holds that tropical regions diversify faster due to higher rates of speciation (caused by increased opportunities for the evolution of reproductive isolation, or faster molecular evolution, or the increased importance of biotic interactions), or due to lower extinction rates. There is phylogenetic evidence for higher rates of diversification in tropical clades, and palaeontological data demonstrate higher rates of origination for tropical taxa, but mixed evidence for latitudinal differences in extinction rates. Studies of latitudinal variation in incipient speciation also suggest faster speciation in the tropics. Distinguishing the roles of history, speciation and extinction in the origin of the latitudinal gradient represents a major challenge to future research.     

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.     

Sequential colonization and diversification of Galapágos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora)

Species richness on island or islandlike systems is a function of colonization, within-island speciation, and extinction. Here we evaluate the relative importance of the first two of these processes as a function of the biogeographical and ecological attributes of islands using the Galápagos endemic land snails of the genus Bulimulus, the most species-rich radiation of these islands. Species in this clade have colonized almost all major islands and are found in five of the six described vegetation zones. We use molecular phylogenetics (based on COI and ITS 1 sequence data) to infer the diversification patterns of extant species of Bulimulus, and multiple regression to investigate the causes of variation among islands in species richness. Maximum-likelihood, Bayesian, and maximum-parsimony analyses yield well-resolved trees with similar topologies. The phylogeny obtained supports the progression rule hypothesis, with species found on older emerged islands connecting at deeper nodes. For all but two island species assemblages we find support for only one or two colonization events, indicating that within-island speciation has an important role in the formation of species on these islands. Even though speciation through colonization is not common, island insularity (distance to nearest major island) is a significant predictor of species richness resulting from interisland colonization alone. However, island insularity has no effect on the overall bulimulid species richness per island. Habitat diversity (measured as plant species diversity), island elevation, and island area, all of which are indirect measures of niche space, are strong predictors of overall bulimulid land snail species richness. Island age is also an important independent predictor of overall species richness, with older islands harboring more species than younger islands. Taken together, our results demonstrate that the diversification of Galápagos bulimulid land snails has been driven by a combination of geographic factors (island age, size, and location), which affect colonization patterns, and ecological factors, such as plant species diversity, that foster within-island speciation.     

How bird clades diversify in response to climatic and geographic factors

While the environmental correlates of global patterns in standing species richness are well understood, it is poorly known which environmental factors promote diversification (speciation minus extinction) in clades. We tested several hypotheses for how geographic and climatic variables should affect diversification using a large dataset of bird sister genera endemic to the New World. We found support for the area, evolutionary speed, environmental predictability and climatic stability hypotheses, but productivity and topographic complexity were rejected as explanations. Genera that had accumulated more species tend to occupy wider niche space, manifested both as occurrence over wider areas and in more habitats. Genera with geographic ranges that have remained more stable in response to glacial‐interglacial changes in climate were also more species rich. Since many relevant explanatory variables vary latitudinally, it is crucial to control for latitude when testing alternative mechanistic explanations for geographic variation in diversification among clades.     

Diversification rates have declined in the Malagasy herpetofauna

The evolutionary origins of Madagascar''s biodiversity remain mysterious despite the fact that relative to land area, there is no other place with consistently high levels of species richness and endemism across a range of taxonomic levels. Most efforts to explain diversification on the island have focused on geographical models of speciation, but recent studies have begun to address the island''s accumulation of species through time, although with conflicting results. Prevailing hypotheses for diversification on the island involve either constant diversification rates or scenarios where rates decline through time. Using relative-time-calibrated phylogenies for seven endemic vertebrate clades and a model-fitting framework, I find evidence that diversification rates have declined through time on Madagascar. I show that diversification rates have clearly declined throughout the history of each clade, and models invoking diversity-dependent reductions to diversification rates best explain the diversification histories for each clade. These results are consistent with the ecological theory of adaptive radiation, and, coupled with ancillary observations about ecomorphological and life-history evolution, strongly suggest that adaptive radiation was an important formative process for one of the most species-rich regions on the Earth. These results cast the Malagasy biota in a new light and provide macroevolutionary justification for conservation initiatives.