Variation In Diversification Rates Research Articles

Evolution of the latitudinal diversity gradient in the hyperdiverse ant genus Pheidole

AbstractAimThe latitudinal diversity gradient is the dominant geographic pattern of life on Earth, but a consensus understanding of its origins has remained elusive. The analysis of recently diverged, hyper‐rich invertebrate groups provides an opportunity to investigate latitudinal patterns with the statistical power of large trees while minimizing potentially confounding variation in ecology and history. Here, we synthesize global phylogenetic and macroecological data on a hyperdiverse (> 1,100 species) ant radiation, Pheidole and test predictions of three general explanations for the latitudinal gradient: variation in diversification rates, tropical conservatism and ecological regulation.LocationGlobal.Time periodThe past 35 million years.Major taxa studiedThe hyperdiverse ant genus Pheidole Westwood.MethodsWe assembled geographic data for 1,499 species and morphospecies, and inferred a dated phylogeny for 449 species of Pheidole, including 167 species newly sequenced for this study. We tested for correlations between diversification rate and latitude with Bayesian analysis of macroevolutionary mixtures (BAMM), hidden state speciation and extinction (HiSSE), geographic state speciation and extinction (GeoSSE), and a non‐parametric method (FiSSE), evaluated evidence for richness steady state, and examined patterns of diversification as Pheidole spread around the globe.ResultsThere was no evidence of systematic variation of net diversification rates with latitude across any of the methods. We found that Pheidole diversification occurred in bursts when new continents were colonized, followed by a slowdown in each region, but there is no evidence richness has saturated at an equilibrium in any region. Additionally, we found latitudinal affinity is moderately conserved with a Neotropical ancestor and simulations show that phylogenetic inertia alone is sufficient to produce the gradient pattern.Main conclusionsOur results provide no evidence that diversification rates vary systematically with latitude. Richness is far from steady state in each region, contrary to the ecological regulation hypothesis, although there is evidence that ecological opportunity promotes diversification after colonization of new areas. The fact that niche conservatism is strong enough to produce the gradient pattern is in accord with the tropical conservatism hypothesis. Overall, these results shed light on the mechanisms underlying the emergence of the diversity gradient within the past 34 million years, complementing recent work on deeper time‐scales, and more generally contribute toward much‐needed invertebrate perspective on global biodiversity dynamics.

Why are red flowers so rare? Testing the macroevolutionary causes of tippiness.

Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short-term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red-flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE (Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSE model when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population-level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.

Evolutionary and ecological success is decoupled in mammals.

AimTo identify which factors distinguish ecologically successful mammalian clades (i.e., clades with a large combined range size) from less successful ones.LocationGlobal.MethodsWe estimated the total range sizes for each individual mammalian subfamily and used phylogenetic regressions to identify the relative importance of factors related to colonization ability (body size and niche width) and adaptability (rate of evolution of body size and rate of evolution of climatic preference) in determining these ranges. We then estimated the importance of the same factors on the variation in diversification rate within mammals.ResultsWe found strong support for a link between total range size and traits related to colonization ability. In particular, we found larger total range sizes among clades containing larger bodied species and clades with wider climatic niche width, while we did not find support for any predictors related to adaptability being linked to total range size. We also found that traits related to increased range size were associated with reduced diversification rate.Main ConclusionsRange size for mammalian clades is mainly predicted by colonization ability, suggesting that most clades are limited by dispersal rather than their ability to adapt to new environments. The most ecologically successful (i.e., most widespread) mammalian clades tend to possess traits that reduce geographical isolation among populations, but the same traits tend to decrease diversification rates. Our results unveil a decoupling between evolutionary and ecological success in mammals.

Species-Specific Means and Within-Species Variance in Glucocorticoid Hormones and Speciation Rates in Birds

At macroevolutionary scales, stress physiology may have consequences for species diversification and subspecies richness. Populations that exploit new resources or undergo range expansion should cope with new environmental challenges, which could favor higher mean stress responses. Within-species variation in the stress response may also play a role in mediating the speciation process: in species with broad variation, there will always be some individuals that can tolerate an unpredictable environment, whereas in species with narrow variation there will be fewer individuals that are able to thrive in a new ecological niche. We tested for the evolutionary relationship between stress response, speciation rate, and subspecies richness in birds by relying on the HormoneBase repository, from which we calculated within- and among-species variation in baseline (BL) and stress-induced (SI) corticosterone levels. To estimate speciation rates, we applied Bayesian analysis of macroevolutionary mixtures that can account for variation in diversification rate among clades and through time. Contrary to our predictions, lineages with higher diversification rates were not characterized by higher BL or SI levels of corticosterone either at the tips or at the deeper nodes of the phylogeny. We also found no association between mean hormone levels and subspecies richness. Within-species variance in corticosterone levels showed close to zero repeatability, thus it is highly unlikely that this is a species-specific trait that influences diversification rates. These results imply that stress physiology may play a minor, if any, role in determining speciation rates in birds.

The Tortoise and the Finch: Testing for island effects on diversification using two iconic Galápagos radiations

AbstractAimsIslands are widely recognized as natural laboratories for evolutionary studies, but many questions about evolution on islands remain unresolved. Here we address two general questions from a macroevolutionary perspective. First, do lineages on islands have increased diversification rates relative to mainland lineages? Second, does the same geographical context (e.g., same archipelago) have similar effects on diversification in unrelated groups? We focused on Darwin's finches and Galápagos tortoises, two endemic radiations from the Galápagos Islands, and the larger families in which they are embedded.LocationGlobal.MethodsWe estimated a new time‐calibrated phylogeny for tortoises (Testudinidae). Then, we examined their macroevolutionary patterns and compared them to those of Darwin's finches and relatives (Thraupidae), using a published thraupid tree. Specifically, we estimated and compared diversification rates between islands and the mainland and between the Galapagos Islands and all other regions, using clade‐based and species‐based approaches.ResultsContrary to expectations, occurrence on islands in general did not significantly increase diversification rates in tanagers or tortoises. However, occurrence in the Galápagos Islands in particular was associated with increased speciation and diversification rates, and explained ~28% of the variation in diversification rates for thraupids and ~46% for testudinids. Both Darwin's finches and Galápagos tortoises were unique within each family in exhibiting the highest diversification rates. The congruence of these macroevolutionary patterns between both radiations supports a strong “place‐dependent” effect on diversification associated with the Galápagos. Finally, we found that Darwin's finches diversified ~2–8 times faster than Galápagos tortoises.Main conclusionsOur results show that occurring on islands in general did not increase diversification rates in these clades, but occurrence in the Galápagos did. We also show that dramatic local‐scale differences in diversification rates between clades in the Galápagos parallel global‐scale differences in diversification rates between these families and between birds and turtles overall.

Climatic niche divergence drives patterns of diversification and richness among mammal families

A major goal of evolutionary biology is to understand why clades differ dramatically in species richness. A key to this challenge is to uncover the correlates of variation in diversification rate (speciation – extinction) among clades. Here, we explore the relationship between diversification rates and the climatic niches of species and clades among 92 families of terrestrial mammals. We use a time-calibrated molecular phylogeny of mammals and climatic data from 3335 species. We show that considerable variation in net diversification rates among mammal families is explained by niche divergence (59%) and rates of niche change (51%). Diversification rates in turn explain most variation in species richness among families (79%). Contrary to expectations, patterns of diversification are not explained by differences in geographic range areas of clades, nor by their climatic niche position (i.e. whether they are primarily tropical or temperate). Overall, these results suggest that speciation through climatic niche divergence may help drive large-scale patterns of diversification and richness. Our results help explain diversification patterns in a major clade of vertebrates, and suggest that similar underlying principles may explain the diversification of many terrestrial clades.

Ecological opportunity may facilitate diversification in Palearctic freshwater organisms: a case study on hydrobiid gastropods

BackgroundDifferences in species richness among phylogenetic clades are attributed to clade age and/or variation in diversification rates. Access to ecological opportunity may trigger a temporary increase in diversification rates and ecomorphological variation. In addition, lower body temperatures in poikilothermic animals may result in decreasing speciation rates as proposed by the metabolic theory of ecology. For strictly freshwater organisms, environmental gradients within a river continuum, linked to elevation and temperature, might promote access to ecological opportunity and alter metabolic rates, eventually influencing speciation and extinction processes. To test these hypotheses, we investigated the influence of environmental temperature and elevation, as proxies for body temperature and ecological opportunity, respectively, on speciation rates and ecomorphological divergence. As model systems served two closely related gastropod genera with unequal species richness and habitat preferences – Pseudamnicola and Corrosella.ResultsLineage-through-time plots and Bayesian macroevolutionary modeling evidenced that Pseudamnicola species, which typically live in lower reaches of rivers, displayed significantly elevated speciation rates in comparison to the ‘headwater genus’ Corrosella. Moreover, state-dependent speciation models suggested that the speciation rate increased with decreasing elevation, supporting the ecological opportunity hypothesis. In contrast, a significant effect of environmental temperature, as proposed by the metabolic theory of ecology, could not be observed. Disparity-through-time plots, models of ecomorphological evolution, and ancestral habitat estimation showed for Pseudamnicola species rapid morphological divergence shortly after periods of elevational and habitat divergence. In contrast, Corrosella species did not deviate from null models of drift-like evolution.ConclusionOur finding that speciation rates are correlated with elevation and ecomorphological disparity but not with environmental temperatures suggests that differences in ecological opportunity may have played a key role in Corrosella and Pseudamnicola diversifications. We propose that Pseudamnicola lineages experienced higher ecological opportunity through dispersal to new locations or habitats in lowlands, which may explain the increase in speciation rates and morphological change. In contrast, the evolution of Corrosella in headwaters is likely less facilitated by the environment and more by non-ecological processes.

Digging their own macroevolutionary grave: fossoriality as an evolutionary dead end in snakes.

The tree of life is highly asymmetrical in its clade wise species richness, and this has often been attributed to variation in diversification rates either across time or lineages. Variations across lineages are usually associated with traits that increase lineage diversification. Certain traits can also hinder diversification by increasing extinction, and such traits are called evolutionary dead ends. Ecological specialization has usually been considered as an evolutionary dead end. However, recent analyses of specializations along single axes have provided mixed support for this model. Here, we test if fossoriality, a trait that forces specialization at multiple axes, acts as an evolutionary dead end in squamates (lizards and snakes) using recently developed phylogenetic comparative methods. We show that fossoriality is an evolutionary dead end in snakes but not in lizards. Fossorial snakes exhibit reduced speciation and increased extinction compared to nonfossorial snakes. Our analysis also indicates that transition rates from fossoriality to nonfossoriality in snakes are significantly lower than transition rates from nonfossoriality to fossoriality. Overall our results suggest that broad-scale ecological interactions that lead to specialization at multiple axes limit diversification.

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

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

Plant size: a key determinant of diversification?

Explaining the variation in diversification rate across groups of plants has long been an important goal of botanists. In plants, complex scenarios involving a combination of extrinsic opportunities and intrinsic traits have been used to explain rapid diversification in certain groups. However, we feel that a very simple trait has been neglected from theories of plant diversification, namely plant height. Here, we argue that decreasing plant size should generally lead to an increase in speciation rate and a decrease in extinction rate. Theory suggests that all population genetic processes involved in speciation are influenced by plant size and its correlates, including seed dispersal distance, population size, generation time and the spatial scale at which plants perceive environmental heterogeneity. In addition, several of these variables, notably population size, also influence rates of extinction. We support our arguments with an empirical analysis showing that plant height is indeed negatively correlated with net diversification rate across families of angiosperms. Finally, we outline how the finer aspects of our hypothesis could be tested, at both micro- and macroevolutionary scales. In addition to strengthening our understanding of the effect of plant size on evolutionary processes, such a research agenda should contribute novel insights to speciation theory in general.

Microhabitat and Climatic Niche Change Explain Patterns of Diversification among Frog Families.

A major goal of ecology and evolutionary biology is to explain patterns of species richness among clades. Differences in rates of net diversification (speciation minus extinction over time) may often explain these patterns, but the factors that drive variation in diversification rates remain uncertain. Three important candidates are climatic niche position (e.g., whether clades are primarily temperate or tropical), rates of climatic niche change among species within clades, and microhabitat (e.g., aquatic, terrestrial, arboreal). The first two factors have been tested separately in several studies, but the relative importance of all three is largely unknown. Here we explore the correlates of diversification among families of frogs, which collectively represent ∼88% of amphibian species. We assemble and analyze data on phylogeny, climate, and microhabitat for thousands of species. We find that the best-fitting phylogenetic multiple regression model includes all three types of variables: microhabitat, rates of climatic niche change, and climatic niche position. This model explains 67% of the variation in diversification rates among frog families, with arboreal microhabitat explaining ∼31%, niche rates ∼25%, and climatic niche position ∼11%. Surprisingly, we show that microhabitat can have a much stronger influence on diversification than climatic niche position or rates of climatic niche change.

Global dynamics of dispersal and diversification among passerine birds

Explaining global variation in geographic and taxonomic diversity gradients represents a central focus of macroecology and macroevolution. Ultimately, these diversity gradients have been generated over deep timescales as a consequence of historical variation in rates of dispersal, diversification, and the capacity of different geographic areas to preserve taxa through time. Here, I assess the relationships among these processes, to elucidate the causes of geographic and taxonomic variation in species richness among the most speciose order of birds: the Passeriformes (c. 6,500 species). To achieve this, I comparatively analyze phylogenetic, distributional and eco-morphological trait data collated at broad taxonomic and spatial scales. The results of my analyses strongly support the prevalence of historical dispersal events across large geographic scales, in addition to spatiotemporal variation in diversification rates. These findings reflect that some lineages and some geographic regions (notably tropical mountain regions and island archipelagoes) generate and maintain a much larger amount of species diversity than others. In addition, the evolution of particular life-history and eco-morphological traits, specifically pair breeding systems, and higher wing aspect-ratios, increased rates of range expansion and diversification. In summary, geographic variation in historical diversification combined with differences in the capacity of lineages to colonize new areas, determines spatial and taxonomic differences in passerine species richness.

Is BAMM Flawed? Theoretical and Practical Concerns in the Analysis of Multi-Rate Diversification Models.

Bayesian analysis of macroevolutionary mixtures (BAMM) is a statistical framework that uses reversible jump Markov chain Monte Carlo to infer complex macroevolutionary dynamics of diversification and phenotypic evolution on phylogenetic trees. A recent article by Moore et al. (MEA) reported a number of theoretical and practical concerns with BAMM. Major claims from MEA are that (i) BAMM’s likelihood function is incorrect, because it does not account for unobserved rate shifts; (ii) the posterior distribution on the number of rate shifts is overly sensitive to the prior; and (iii) diversification rate estimates from BAMM are unreliable. Here, we show that these and other conclusions from MEA are generally incorrect or unjustified. We first demonstrate that MEA’s numerical assessment of the BAMM likelihood is compromised by their use of an invalid likelihood function. We then show that “unobserved rate shifts” appear to be irrelevant for biologically plausible parameterizations of the diversification process. We find that the purportedly extreme prior sensitivity reported by MEA cannot be replicated with standard usage of BAMM v2.5, or with any other version when conventional Bayesian model selection is performed. Finally, we demonstrate that BAMM performs very well at estimating diversification rate variation across the n}{}{sim}20% of simulated trees in MEA’s data set for which it is theoretically possible to infer rate shifts with confidence. Due to ascertainment bias, the remaining 80% of their purportedly variable-rate phylogenies are statistically indistinguishable from those produced by a constant-rate birth–death process and were thus poorly suited for the summary statistics used in their performance assessment. We demonstrate that inferences about diversification rates have been accurate and consistent across all major previous releases of the BAMM software. We recognize an acute need to address the theoretical foundations of rate-shift models for phylogenetic trees, and we expect BAMM and other modeling frameworks to improve in response to mathematical and computational innovations. However, we remain optimistic that that the imperfect tools currently available to comparative biologists have provided and will continue to provide important insights into the diversification of life on Earth.

Asymmetric geographic range expansion explains the latitudinal diversity gradients of four major taxa of marine plankton

AbstractExtensive investigation of the close association between biological diversity and environmental temperature has not yet yielded a generally accepted, empirically validated mechanism to explain latitudinal gradients of species diversity, which occur in most taxa. Using the highly resolved late Cenozoic fossil records of four major taxa of marine plankton, we show that their gradients arise as a consequence of asymmetric geographic range expansion rather than latitudinal variation in diversification rate, as commonly believed. Neither per capita speciation nor extinction rates trend significantly with temperature or latitude for these marine plankton. Species of planktonic foraminifera and calcareous nannoplankton that originate in the temperate zone preferentially spread toward and arrive earlier in the tropics to produce a normal gradient with tropical diversity peaks; by contrast, temperate-zone originating species of diatoms and radiolarians preferentially spread toward and arrive earlier in polar regions to produce reversed gradients with high-latitude diversity peaks. Our results suggest that temperature affects latitudinal diversity gradients chiefly by its effect on species’ range limits rather than on probabilities of speciation and extinction. We show that this mechanism also appears to operate in various multicellular taxa, thus providing a widely applicable explanation for the origin of latitudinal diversity gradients.

What explains patterns of biodiversity across the Tree of Life?: New research is revealing the causes of the dramatic variation in species numbers across branches of the Tree of Life.

A major challenge in biology is to explain why some groups have thousands or millions of species whereas others have few. Here, I review the causes of this variation. New studies reveal that higher species numbers in many major groups are explained by higher diversification rates (and traits that accelerate these rates). These traits span most of biology (e.g. genomics, ecology, morphology). Rather than simply testing individual traits, research should now focus on comparing how much variation in diversification rates is explained by different types of traits. For example, is local-scale ecology (e.g. microhabitat, diet) more important than large-scale climate (e.g. occurring in tropical vs. temperate regions)? Are traits based on particular values (e.g. smaller body sizes) more important than those based on rates of change (e.g. faster size evolution)? I review recent results on the relative importance of different traits for driving diversification, and present a framework for future research.

What Explains Patterns of Diversification and Richness among Animal Phyla?

Animal phyla vary dramatically in species richness (from one species to >1.2 million), but the causes of this variation remain largely unknown. Animals have also evolved striking variation in morphology and ecology, including sessile marine taxa lacking heads, eyes, limbs, and complex organs (e.g., sponges), parasitic worms (e.g., nematodes, platyhelminths), and taxa with eyes, skeletons, limbs, and complex organs that dominate terrestrial ecosystems (arthropods, chordates). Relating this remarkable variation in traits to the diversification and richness of animal phyla is a fundamental yet unresolved problem in biology. Here, we test the impacts of 18 traits (including morphology, ecology, reproduction, and development) on diversification and richness of extant animal phyla. Using phylogenetic multiple regression, the best-fitting model includes five traits that explain ∼74% of the variation in diversification rates (dioecy, parasitism, eyes/photoreceptors, a skeleton, nonmarine habitat). However, a model including just three (skeleton, parasitism, habitat) explains nearly as much variation (∼67%). Diversification rates then largely explain richness patterns. Our results also identify many striking traits that have surprisingly little impact on diversification (e.g., head, limbs, and complex circulatory and digestive systems). Overall, our results reveal the key factors that shape large-scale patterns of diversification and richness across >80% of all extant, described species.

Diversification rates and species richness across the Tree of Life.

Species richness varies dramatically among clades across the Tree of Life, by over a million-fold in some cases (e.g. placozoans versus arthropods). Two major explanations for differences in richness among clades are the clade-age hypothesis (i.e. species-rich clades are older) and the diversification-rate hypothesis (i.e. species-rich clades diversify more rapidly, where diversification rate is the net balance of speciation and extinction over time). Here, we examine patterns of variation in diversification rates across the Tree of Life. We address how rates vary across higher taxa, whether rates within higher taxa are related to the subclades within them, and how diversification rates of clades are related to their species richness. We find substantial variation in diversification rates, with rates in plants nearly twice as high as in animals, and rates in some eukaryotes approximately 10-fold faster than prokaryotes. Rates for each kingdom-level clade are then significantly related to the subclades within them. Although caution is needed when interpreting relationships between diversification rates and richness, a positive relationship between the two is not inevitable. We find that variation in diversification rates seems to explain most variation in richness among clades across the Tree of Life, in contrast to the conclusions of previous studies.

A Bayesian approach for detecting the impact of mass‐extinction events on molecular phylogenies when rates of lineage diversification may vary

SummaryThe paleontological record chronicles numerous episodes of mass extinction that severely culled the Tree of Life. Biologists have long sought to assess the extent to which these events may have impacted particular groups. We present a novel method for detecting the impact of mass‐extinction events on molecular phylogenies, even in the presence of tree‐wide diversification‐rate variation and in the absence of additional information from the fossil record.Our approach is based on an episodic stochastic‐branching process model in which rates of speciation and extinction are constant between events. We model three types of events: (i) instantaneous tree‐wide shifts in speciation rate; (ii) instantaneous tree‐wide shifts in extinction rate and (iii) instantaneous tree‐wide mass‐extinction events. Each type of event is modelled as an independent compound Poisson process (CPP), where the waiting times between events are exponentially distributed with event‐specific rate parameters. The magnitude of each event is drawn from an event‐specific prior distribution. Parameters of the model are then estimated in a Bayesian statistical framework using a reversible‐jump Markov chain Monte Carlo algorithm. This Bayesian approach enables us to distinguish between tree‐wide diversification‐rate variation and mass‐extinction events by specifying a biologically informed prior on the magnitude of mass‐extinction events and empirical hyperpriors on the diversification‐rate parameters.We demonstrate via simulation that this method has substantial power to detect the number of mass‐extinction events and provides unbiased estimates of the timing of mass‐extinction events, while exhibiting an appropriate (i.e. <5%) false‐discovery rate, even when background diversification rates vary. Finally, we provide an empirical demonstration of this approach, which reveals that conifers experienced a major episode of mass extinction ≈23 Ma.This new approach – the CPP on Mass‐Extinction Times (CoMET) model – provides an effective tool for detecting the impact of mass‐extinction events on molecular phylogenies, even when the history of those groups includes temporal variation in diversification rates and when the fossil history of those groups is poorly known.

Testing the Relationships between Diversification, Species Richness, and Trait Evolution.

Understanding which traits drive species diversification is essential for macroevolutionary studies and to understand patterns of species richness among clades. An important tool for testing if traits influence diversification is to estimate rates of net diversification for each clade, and then test for a relationship between traits and diversification rates among clades. However, this general approach has become very controversial. Numerous papers have now stated that it is inappropriate to analyze net diversification rates in groups in which clade richness is not positively correlated with clade age. Similarly, some have stated that variation in net diversification rates does not explain variation in species richness patterns among clades across the Tree of Life. Some authors have also suggested that strong correlations between richness and diversification rates are a statistical artifact and effectively inevitable. If this latter point is true, then correlations between richness and diversification rates would be uninformative (or even misleading) for identifying how much variation in species richness among clades is explained by variation in net diversification rates. Here, we use simulations (based on empirical data for plethodontid salamanders) to address three main questions. First, how is variation in net diversification rates among clades related to the relationship between clade age and species richness? Second, how accurate are these net diversification rate estimators, and does the age-richness relationship have any relevance to their accuracy? Third, is a relationship between species richness and diversification rates an inevitable, statistical artifact? Our simulations show that strong, positive age-richness relationships arise when diversification rates are invariant among clades, whereas realistic variation in diversification rates among clades frequently disrupts this relationship. Thus, a significant age-richness relationship should not be a requirement for utilizing net diversification rates in macroevolutionary studies. Moreover, we find no difference in the accuracy of net diversification rate estimators between conditions in which there are strong, positive relationships between clade age and richness and conditions in which these strong relationships are absent. We find that net diversification rate estimators are reasonably accurate under many conditions (true and estimated rates are strongly corrrelated, and typically differ by ∼10-20%), but become more accurate when clades are older and less accurate when using incorrect assumptions about extinction. We also find that significant relationships between richness and diversification rates fail to arise under many conditions, especially when there are faster rates in younger clades. Therefore, a significant relationship between richness and diversification rates is not inevitable. Given this latter result, we suggest that relationships between richness and diversification should be tested for when attempting to explain the causes of richness patterns, to avoid potential misinterpretations (e.g., high diversification rates associated with low-richness clades). Similarly, our results also provide some support for previous studies suggesting that variation in diversification rates might explain much of the variation in species richness among major clades, based on strong relationships between clade richness and diversification rates.

Multi-locus phylogeny and divergence time estimates of Enallagma damselflies (Odonata: Coenagrionidae)

Reconstructing evolutionary patterns of species and populations provides a framework for asking questions about the impacts of climate change. Here we use a multilocus dataset to estimate gene trees under maximum likelihood and Bayesian models to obtain a robust estimate of relationships for a genus of North American damselflies, Enallagma. Using a relaxed molecular clock, we estimate the divergence times for this group. Furthermore, to account for the fact that gene tree analyses can overestimate ages of population divergences, we use a multi-population coalescent model to gain a more accurate estimate of divergence times. We also infer diversification rates using a method that allows for variation in diversification rate through time and among lineages. Our results reveal a complex evolutionary history of Enallagma, in which divergence events both predate and occur during Pleistocene climate fluctuations. There is also evidence of diversification rate heterogeneity across the tree. These divergence time estimates provide a foundation for addressing the relative significance of historical climatic events in the diversification of this genus.