Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity

Many groups show higher species richness in tropical regions but the underlying causes remain unclear. Despite many competing hypotheses to explain latitudinal diversity gradients, only three processes can directly change species richness across regions: speciation, extinction and dispersal. These processes can be addressed most powerfully using large-scale phylogenetic approaches, but most previous studies have focused on small groups and recent time scales, or did not separate speciation and extinction rates. We investigate the origins of high tropical diversity in amphibians, applying new phylogenetic comparative methods to a tree of 2871 species. Our results show that high tropical diversity is explained by higher speciation in the tropics, higher extinction in temperate regions and limited dispersal out of the tropics compared with colonization of the tropics from temperate regions. These patterns are strongly associated with climate-related variables such as temperature, precipitation and ecosystem energy. Results from models of diversity dependence in speciation rate suggest that temperate clades may have lower carrying capacities and may be more saturated (closer to carrying capacity) than tropical clades. Furthermore, we estimate strikingly low tropical extinction rates over geological time scales, in stark contrast to the dramatic losses of diversity occurring in tropical regions presently.     

Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity

Why are there more species in the tropics than in temperate regions? In recent years, this long-standing question has been addressed primarily by seeking environmental correlates of diversity. But to understand the ultimate causes of diversity patterns, we must also examine the evolutionary and biogeographic processes that directly change species numbers (i.e., speciation, extinction, and dispersal). With this perspective, we dissect the latitudinal diversity gradient in hylid frogs. We reconstruct a phylogeny for 124 hylid species, estimate divergence times and diversification rates for major clades, reconstruct biogeographic changes, and use ecological niche modeling to identify climatic variables that potentially limit dispersal. We find that hylids originated in tropical South America and spread to temperate regions only recently (leaving limited time for speciation). There is a strong relationship between the species richness of each region and when that region was colonized but not between the latitudinal positions of clades and their rates of diversification. Temperature seasonality seemingly limits dispersal of many tropical clades into temperate regions and shows significant phylogenetic conservatism. Overall, our study illustrates how two general principles (niche conservatism and the time-for-speciation effect) may help explain the latitudinal diversity gradient as well as many other diversity patterns across taxa and regions.     

EVOLUTIONARY AND BIOGEOGRAPHIC ORIGINS OF HIGH TROPICAL DIVERSITY IN OLD WORLD FROGS (RANIDAE)

Differences in species richness between regions are ultimately explained by patterns of speciation, extinction, and biogeographic dispersal. Yet, few studies have considered the role of all three processes in generating the high biodiversity of tropical regions. A recent study of a speciose group of predominately New World frogs (Hylidae) showed that their low diversity in temperate regions was associated with relatively recent colonization of these regions, rather than latitudinal differences in diversification rates (rates of speciation–extinction). Here, we perform parallel analyses on the most species-rich group of Old World frogs (Ranidae; ∼1300 species) to determine if similar processes drive the latitudinal diversity gradient. We estimate a time-calibrated phylogeny for 390 ranid species and use this phylogeny to analyze patterns of biogeography and diversification rates. As in hylids, we find a strong relationship between the timing of colonization of each region and its current diversity, with recent colonization of temperate regions from tropical regions. Diversification rates are similar in tropical and temperate clades, suggesting that neither accelerated tropical speciation rates nor greater temperate extinction rates explain high tropical diversity in this group. Instead, these results show the importance of historical biogeography in explaining high species richness in both the New World and Old World tropics.     

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'.     

Faster Speciation and Reduced Extinction in the Tropics Contribute to the Mammalian Latitudinal Diversity Gradient

The increase in species richness from the poles to the tropics, referred to as the latitudinal diversity gradient, is one of the most ubiquitous biodiversity patterns in the natural world. Although understanding how rates of speciation and extinction vary with latitude is central to explaining this pattern, such analyses have been impeded by the difficulty of estimating diversification rates associated with specific geographic locations. Here, we use a powerful phylogenetic approach and a nearly complete phylogeny of mammals to estimate speciation, extinction, and dispersal rates associated with the tropical and temperate biomes. Overall, speciation rates are higher, and extinction rates lower, in the tropics than in temperate regions. The diversity of the eight most species-rich mammalian orders (covering 92% of all mammals) peaks in the tropics, except that of the Lagomorpha (hares, rabbits, and pikas) reaching a maxima in northern-temperate regions. Latitudinal patterns in diversification rates are strikingly consistent with these diversity patterns, with peaks in species richness associated with low extinction rates (Primates and Lagomorpha), high speciation rates (Diprotodontia, Artiodactyla, and Soricomorpha), or both (Chiroptera and Rodentia). Rates of range expansion were typically higher from the tropics to the temperate regions than in the other direction, supporting the “out of the tropics” hypothesis whereby species originate in the tropics and disperse into higher latitudes. Overall, these results suggest that differences in diversification rates have played a major role in shaping the modern latitudinal diversity gradient in mammals, and illustrate the usefulness of recently developed phylogenetic approaches for understanding this famous yet mysterious pattern.     

Global patterns of diversification and species richness in amphibians

Geographic patterns of species richness ultimately arise through the processes of speciation, extinction, and dispersal, but relatively few studies consider evolutionary and biogeographic processes in explaining these diversity patterns. One explanation for high tropical species richness is that many species-rich clades originated in tropical regions and spread to temperate regions infrequently and more recently, leaving little time for species richness to accumulate there (assuming similar rates of diversification in temperate and tropical regions). However, the major clades of anurans (frogs) and salamanders may offer a compelling counterexample. Most salamander families are predominately temperate in distribution, but the one primarily tropical clade (Bolitoglossinae) contains nearly half of all salamander species. Similarly, most basal clades of anurans are predominately temperate, but one largely tropical clade (Neobatrachia) contains approximately 96% of anurans. In this article, I examine patterns of diversification in frogs and salamanders and their relationship to large-scale patterns of species richness in amphibians. I find that diversification rates in both frogs and salamanders increase significantly with decreasing latitude. These results may shed light on both the evolutionary causes of the latitudinal diversity gradient and the dramatic but poorly explained disparities in the diversity of living amphibian clades.     

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.     

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.     

Environmental predictors of global parrot (Aves: Psittaciformes) species richness and phylogenetic diversity

Aim Spatial patterns of phylogenetic diversity (PD) aid our ability to discern diversification rate mechanisms underlying hypotheses for the large‐scale distribution of biodiversity. We develop a predictive framework for the way in which spatial patterns of PD vary with those of species richness, depending on the balance between speciation and extinction rates. Within this framework, diversification processes thought to underlie the productive energy, ambient energy, topographic variability and habitat variety hypotheses predict that gradients of increase in species richness will be associated with: (1) decreasing extinction rates where driven by productive energy, hence increasing relative PD (i.e. PD controlling for species richness, or PD_rel); (2) a similar positive relationship between ambient energy and PD_rel; (3) increasing speciation rates where driven by topographic variability, hence decreasing PD_rel; and (4) no consistent relationship between PD_rel and habitat variety when driven by the latter. We test these predictions using distributional data on parrots. Location Neotropical, Afrotropical, Indo‐Malayan and Australasian realms. Methods Spatial models were used to test the predictions. Results Globally, a positive association between productive energy and PD_rel confirms prediction (1). However, within realms, hump‐shaped relationships suggest the importance of decreasing extinction rates up to a threshold level of productive energy, and the increasing importance of speciation rates thereafter. Ambient energy is positively associated with PD_rel in Australasia, Indo‐Malaya, and globally, supporting prediction (2). However, this is driven by the coincidence of highest PD_rel in areas of high ambient energy and intermediate productive energy (i.e. in seasonal tropical environments), which may be characterized by relatively low speciation and extinction rates. In the Neotropics, increasing topographic variability is associated with decreasing PD_rel and increasing species richness, suggesting an increasing gradient of speciation, supporting prediction (3). Elsewhere, the signal of this mechanism may be obscured by collinearities with energy gradients. The lack of an overall relationship between habitat diversity and PD_rel confirms prediction (4). Main conclusions Spatial patterns of PD_rel in relation to environmental gradients may be sensitive to collinearities among those gradients. Nevertheless, patterns emerge which have implications for the relative importance of speciation and extinction processes in generating latitudinal diversity gradients.     

Latitude and rates of diversification in birds and butterflies

Central to many explanations of latitudinal diversity gradients is the idea that rates of species diversification increase towards the equator. However, there have been few explicit tests of whether or not this pattern exists. Using sister-group analyses to compare 48 clades of passerine birds and swallowtail butterflies from different latitudes, I found evidence that relative rates of diversification per unit time are indeed higher towards the equator. This pattern is explicable in terms of abiotic factors which vary continuously with latitude, and may be further enhanced by diversity-dependent speciation and extinction processes.     

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.     

Diversification rates and the latitudinal gradient of diversity in mammals

The latitudinal gradient of species richness has frequently been attributed to higher diversification rates of tropical groups. In order to test this hypothesis for mammals, we used a set of 232 genera taken from a mammalian supertree and, additionally, we reconstructed dated Bayesian phylogenetic trees of 100 genera. For each genus, diversification rate was estimated taking incomplete species sampling into account and latitude was assigned considering the heterogeneity in species distribution ranges. For both datasets, we found that the average diversification rate was similar among all latitudinal bands. Furthermore, when we used phylogenetically independent contrasts, we did not find any significant correlation between latitude and diversification parameters, including different estimates of speciation and extinction rates. Thus, other factors, such as the dynamics of dispersal through time, may be required to explain the latitudinal gradient of diversity in mammals.     

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.     

Time and environment explain the current richness distribution of non‐marine turtles worldwide

Ecological, historical, and evolutionary hypotheses are important to explain geographical diversity gradients in many clades, but few studies have combined them into a single analysis allowing a comparison of their relative importance. This study aimed to evaluate the relative importance of ecological, historical, and evolutionary hypotheses in explaining the current global distribution of non‐marine turtles, a group whose distribution patterns are still poorly explored. We used data from distribution range maps of 336 species of non‐marine turtles, environmental layers, and phylogeny to obtain richness estimates of these animals in 2° × 2° cells and predictors related to ecological, evolutionary and historical hypotheses driving richness patterns. Then we used a path analysis to evaluate direct and indirect effects of the predictors on turtle richness. Ancestral area reconstruction was also performed in order to evaluate the influence of time‐for‐speciation in the current diversity of the group. We found that environmental variables had the highest direct effects on non‐marine turtle richness, whereas diversification rates and area available in the last 55 million yr minimally influenced turtle distributions. We found evidence for the time‐for‐speciation effect, since regions colonized early were generally richer than recently colonized regions. In addition, regions with a high number of colonization events had a higher number of turtle species. Our results suggested that ecological processes may influence non‐marine turtle richness independent of diversification rates, but they are probably related to dispersal abilities. However, colonization time was also an important component that must be taken into account. Finally, our study provided additional support for the importance of ecological (climate and productivity) and historical (time‐for‐speciation and dispersal) processes in shaping current biodiversity patterns.     

The tropics: cradle,museum or casino? A dynamic null model for latitudinal gradients of species diversity

Several ecological and evolutionary hypotheses have been proposed to explain the latitudinal diversity gradient (LDG), but a general model for this conspicuous pattern remains elusive. Mid-domain effect (MDE) models generate gradients of species diversity by randomly placing the geographic ranges of species in one- or two-dimensional spaces, thus excluding both evolutionary processes and the effect of contemporary climate. Traditional MDE models are statistical and static because they determine the size of ranges either randomly or based on empirical frequency distributions. Here we present a simple dynamic null model for the LDG that simulates stochastic processes of range shifts, extinction and speciation. The model predicts higher species diversity and higher extinction and speciation rates in the tropics, and a strong influence of range movements in shaping the LDG. These null expectations should be taken into consideration in studies aimed at understanding the many factors that generate latitudinal diversity gradients.     

Energy gradients and the geographic distribution of local ant diversity

Geographical diversity gradients, even among local communities, can ultimately arise from geographical differences in speciation and extinction rates. We evaluated three models—energy-speciation, energy-abundance, and area—that predict how geographic trends in net diversification rates generate trends in diversity. We sampled 96 litter ant communities from four provinces: Australia, Madagascar, North America, and South America. The energy-speciation hypothesis best predicted ant species richness by accurately predicting the slope of the temperature diversity curve, and accounting for most of the variation in diversity. The communities showed a strong latitudinal gradient in species richness as well as inter-province differences in diversity. The former vanished in the temperature-diversity residuals, suggesting that the latitudinal gradient arises primarily from higher diversification rates in the tropics. However, inter-province differences in diversity persisted in those residuals—South American communities remained more diverse than those in North America and Australia even after the effects of temperature were removed.     

Latitudinal‐diversity gradients can be shaped by biotic processes: new insights from an eco‐evolutionary model

The processes involved in shaping latitudinal‐diversity gradients (LDGs) have been a longstanding source of debate and research. Climatic, historical and evolutionary factors have all been shown to contribute to the formation of LDGs. However, meta‐analyses have shown that different clades have LDG slopes that may vary in more than one order of magnitude. Such large variation cannot be explained solely by climatic or historical factors (e.g. difference in surface area between temperate and tropical zones) given that all clades within a geographic region are subject to the same conditions. Therefore, biotic processes intrinsic to each taxonomic group could be relevant in explaining rate differences in diversity decline across latitudinal gradients among groups. In this study, we developed a model simulating multiple competing species subjected (or not) to a demographic Allee effect. We simulated the range expansion of these species across an environmental gradient to show how these two overlooked factors (competition and Allee effects) are capable of modulating LDGs. Allee effects resulted in a steeper LDG given a higher probability of local extinction and lower colonization capacity compared to species without Allee effects. Likewise, stronger competition also led to a steeper decline in species diversity compared to scenarios with weaker species antagonistic interactions. This pattern occurred mostly due to the strength of priority effects, wherein scenarios with strong competition, species that dispersed earlier in the landscape were able to secure many patches whereas late‐arriving species were progressively precluded from expanding their ranges. Overall, our results suggest that the effect of biotic processes in shaping macroecological patterns could be more important than it is currently appreciated.     

Correlates of diversification in the plant clade Dipsacales: geographic movement and evolutionary innovations

We explore patterns of diversification in the plant clades Adoxaceae and Valerianaceae (within Dipsacales), evaluating correlations between biogeographic change (i.e., movements into new areas), morphological change (e.g., the origin of putative key innovations associated with vegetative and reproductive characters), and shifts in rates of diversification. Our findings indicate that rates of diversification in these plants tend to be less tightly correlated with the evolution of morphological innovations but instead exhibit a pronounced correlation with movement into new geographic areas, particularly the dispersal of lineages into new mountainous regions. The interdependence among apparent novelties (arising from their nested phylogenetic distribution) and the correlation between morphological and biogeographic change suggests a complex history of diversification in Dipsacales. Overall, these findings highlight the importance of incorporating biogeographic history in studies of diversification rates and in the study of geographic gradients in species richness. Furthermore, these results argue against a simple deterministic relationship between dispersal and diversification: like other factors that may influence the probability of speciation and/or extinction, the impact of dispersal on diversification rates depends on being in the right place at the right time.     

ORIGIN AND DIVERSIFICATION OF THE CALIFORNIA FLORA: RE‐EXAMINING CLASSIC HYPOTHESES WITH MOLECULAR PHYLOGENIES

The California Floristic Province exhibits one of the richest floras on the planet, with more than 5500 native plant species, approximately 40% of which are endemic. Despite its impressive diversity and the attention it has garnered from ecologists and evolutionary biologists, historical causes of species richness and endemism in California remain poorly understood. Using a phylogenetic analysis of 16 angiosperm clades, each containing California natives in addition to species found only outside California, we show that CA's current biodiversity primarily results from low extinction rates, as opposed to elevated speciation or immigration rates. Speciation rates in California were lowest among Arcto‐Tertiary lineages (i.e., those colonizing California from the north, during the Tertiary), but extinction rates were universally low across California native plants of all historical, geographic origins. In contrast to long‐accepted ideas, we find that California diversification rates were generally unaffected by the onset of the Mediterranean climate. However, the Mediterranean climate coincided with immigration of many desert species, validating one previous hypothesis regarding origins of CA's plant diversity. This study implicates topographic complexity and climatic buffering as key, long‐standing features of CA's landscape favoring plant species persistence and diversification, and highlights California as an important refuge under changing climates.