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Extinction Rates Should Not Be Estimated from Molecular Phylogenies
Abstract
Molecular phylogenies contain information about the tempo and mode of species diversification through time. Because extinction leaves a characteristic signature in the shape of molecular phylogenetic trees, many studies have used data from extant taxa only to infer extinction rates. This is a promising approach for the large number of taxa for which extinction rates cannot be estimated from the fossil record. Here, I explore the consequences of violating a common assumption made by studies of extinction from phylogenetic data. I show that when diversification rates vary among lineages, simple estimators based on the birth-death process are unable to recover true extinction rates. This is problematic for phylogenetic trees with complete taxon sampling as well as for the simpler case of clades with known age and species richness. Given the ubiquity of variation in diversification rates among lineages and clades, these results suggest that extinction rates should not be estimated in the absence of fossil data.
... We estimated speciation rates with Bayesian Analysis of Macroevolutionary Mixtures (BAMM), implemented with a reversible-jump Markov Chain Monte Carlo (MCMC) framework (26), accounting for incomplete sampling by specifying the fraction of known richness of each genus that was sampled (20). In all analyses with BAMM, we only considered speciation rate, not extinction rate, which avoids potentially unreliable parameter estimation (27)(28)(29) and is predicted to give more accurate estimates of speciation rate variability (30). We found 44-fold variation in the rate of speciation, with 36 core rate shifts in the best shift configuration, each of which indicated significant increases in speciation rate (overall rate heterogeneity: Bayes Factor >100). ...
... We excluded the first 10% of generations as burn-in, and assessed convergence with the R package Coda (110), confirming that the effective sample size of each parameter was >400. We ignored reconstructions of extinction rate, which are known to be unreliable when modeled from phylogenies containing only extant taxa (27). We plotted speciation rates through time against temperature curves for both frameworks and found that the relationship between global cooling and speciation rate was robust in both frameworks (SI Appendix, Fig. S2). ...
Although climate change has been implicated as a major catalyst of diversification, its effects are thought to be inconsistent and much less pervasive than localized climate or the accumulation of species with time. Focused analyses of highly speciose clades are needed in order to disentangle the consequences of climate change, geography, and time. Here, we show that global cooling shapes the biodiversity of terrestrial orchids. Using a phylogeny of 1,475 species of Orchidoideae, the largest terrestrial orchid subfamily, we find that speciation rate is dependent on historic global cooling, not time, tropical distributions, elevation, variation in chromosome number, or other types of historic climate change. Relative to the gradual accumulation of species with time, models specifying speciation driven by historic global cooling are over 700 times more likely. Evidence ratios estimated for 212 other plant and animal groups reveal that terrestrial orchids represent one of the best-supported cases of temperature-spurred speciation yet reported. Employing >2.5 million georeferenced records, we find that global cooling drove contemporaneous diversification in each of the seven major orchid bioregions of the Earth. With current emphasis on understanding and predicting the immediate impacts of global warming, our study provides a clear case study of the long-term impacts of global climate change on biodiversity.
... For instance, detecting whether rates vary through time has been questioned due to difficulties in deciphering whether speciation only or extinction only or both are responsible for rate variation (Liow et al. 2010, Burin et al. 2019. Another issue in birth-death models lies in estimates of extinction rates that do not match those in the fossil record , Rabosky 2010, which is due to recent clades diversifying quickly and masking the signal of extinction in other parts of the phylogeny (Morlon et al. 2011). Here we used the environment-dependent birthdeath approach, an extension of Morlon et al. (2011)'s model, where speciation and extinction can also depend on external environmental variables (Condamine et al. 2013(Condamine et al. , 2019, such as temperature variation through time (see the Supplemental Text). ...
... The role of extinction cannot be ignored, as this evolutionary process represents a component of the net diversification rate shaping diversity dynamics (Morlon 2014). However, extinction rates can be difficult to estimate with phylogenies alone (Rabosky 2010; but see Morlon et al. 2011). The best-fit models did not identify nonzero extinction rates for the eight angiosperm Diversification patterns of selected Amazonian clades. ...
The Amazon hosts one of the largest and richest rainforests in the world, but its origins remain debated. Growing evidence suggests that geodiversity and geological history played essential roles in shaping the Amazonian flora. Here we summarize the geo-climatic history of the Amazon and review paleopalynological records and time-calibrated phylogenies to evaluate the response of plants to environmental change. The Neogene fossil record suggests major sequential changes in plant composition and an overall decline in diversity. Phylogenies of eight Amazonian plant clades paint a mixed picture, with the diversification of most groups best explained by constant speciation rates through time, while others indicate clade-specific increases or decreases correlated with climatic cooling or increasing Andean elevation. Overall, the Amazon forest seems to represent a museum of diversity with a high potential for biological diversification through time. To fully understand how the Amazon got its modern biodiversity, further multidisciplinary studies conducted within a multimillion-year perspective are needed. ▪ The history of the Amazon rainforest goes back to the beginning of the Cenozoic (66 Ma) and was driven by climate and geological forces. ▪ In the early Neogene (23–13.8 Ma), a large wetland developed with episodic estuarine conditions and vegetation ranging from mangroves to terra firme forest. ▪ In the late Neogene (13.8–2.6 Ma), the Amazon changed into a fluvial landscape with a less diverse and more open forest, although the details of this transition remain to be resolved. ▪ These geo-climatic changes have left imprints on the modern Amazonian diversity that can be recovered with dated phylogenetic trees. ▪ Amazonian plant groups show distinct responses to environmental changes, suggesting that Amazonia is both a refuge and a cradle of biodiversity.
... Estimating diversification rates with phylogenies of extant taxa has proved to be powerful, especially as it allows for testing hypotheses related to trait evolution, biogeography and their links with deep-time diversity dynamics [9][10][11] . However, phylogeny-based approaches remain challenging and come with limitations on the taxon sampling, tree size, estimation of extinction, or on the limited identifiability of diversification processes 8,[12][13][14][15] . Although they are useful for studying clades whose fossil record is poor and/or not preserving the biological traits to be studied, it has been shown that considering the fossil record is critical for addressing macroevolutionary questions [16][17][18] . ...
... Fourth, the diversification analyses are performed in a Bayesian framework that allows jointly estimating speciation, extinction, preservation rates, and the rate shifts as well as the magnitude of these rates without phylogeny 23,24,78 . Fifth, this approach would theoretically provide more accurate speciation and extinction rates for the focal group, in particular extinction rates that are often seen as poorly estimated with phylogenies of extant species only 12,17 (but see Morlon et al. 98 ). Both phylogeny-based and fossil occurrence-based analyses converged on a crown age between 208 and 170 Ma for the carcharhiniforms. ...
Estimating deep-time species-level diversification processes remains challenging. Both the fossil record and molecular phylogenies allow the estimation of speciation and extinction rates, but each type of data may still provide an incomplete picture of diversification dynamics. Here, we combine species-level palaeontological (fossil occurrences) and neontological (molecular phylogenies) data to estimate deep-time diversity dynamics through process-based birth–death models for Carcharhiniformes, the most speciose shark order today. Despite their abundant fossil record dating back to the Middle Jurassic, only a small fraction of extant carcharhiniform species is recorded as fossils, which impedes relying only on the fossil record to study their recent diversification. Combining fossil and phylogenetic data, we recover a complex evolutionary history for carcharhiniforms, exemplified by several variations in diversification rates with an early low diversity period followed by a Cenozoic radiation. We further reveal a burst of diversification in the last 30 million years, which is partially recorded with fossil data only. We also find that reef expansion and temperature change can explain variations in speciation and extinction through time. These results pinpoint the primordial importance of these environmental variables in the evolution of marine clades. Our study also highlights the benefit of combining the fossil record with phylogenetic data to address macroevolutionary questions.
... This lack of knowledge may be also due to the challenge of differentiating between evolutionary scenarios based on birth-death models and phylogenies of extant species alone (Nee et al., 1994;Rabosky, 2010). Recent studies have raised concerns on difficulties in identifying parameter values when working with birth-death models under rate variation scenarios (Stadler, 2013;Burin et al., 2019), showing that speciation (birth, λ) and extinction (death, μ) rates sometimes cannot be inferred from molecular phylogenies (Louca and Pennell, 2020). ...
... We found that the species richness of five plant and eight tetrapod clades declined towards the present (e.g., Sideroxylon [Sapotaceae], Guatteria [Annonaceae], caviomorph rodents, Thraupidae birds, or Lophyohylinae [Hylidae] frogs). This proportion might seem minor but is noteworthy when compared with the low support for this model found in the Neotropical literature, which could be explained by the difficulties in inferring negative diversification rates based on molecular phylogenies (Rabosky, 2010). Inferring diversity declines is challenging, and often requires accounting for among-clade rate heterogeneity (Morlon et al., 2011). ...
The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In contrast, diversification dynamics differ across taxa: plant diversity mostly expanded through time (88%), while a substantial fraction (43%) of tetrapod diversity accumulated at a slower pace or declined toward the present. These opposite evolutionary patterns may reflect different capacities for plants and tetrapods to cope with past climate changes.
... Extinct species cannot be observed on such trees in most cases, but extinction is expected to leave characteristic signatures on tree shape and the temporal distribution of branching events, allowing inferences about extinction rates (Nee, Holmes, May, & Harvey, 1994a). In practice, however, extinction rates and extinction fractions have proven difficult to estimate with accuracy and precision, especially in the presence of rate heterogeneity through time and across lineages (Rabosky, 2010(Rabosky, , 2016. Despite this difficulty, net diversification rates and turnover rates, which are functions of speciation and extinction rates, can be estimated with greater confidence (e.g., Beaulieu & O'Meara, 2016;Title & Rabosky, 2019). ...
... It is possible that recent cercopithecoid evolutionary history has been characterized by low rates of extinction as the modern genera have radiated in response to changes in regional environments and primate extinctions associated with Plio-Pleistocene climatic fluctuations (Elton, 2007;Elton & Dunn, 2020;Roos et al., 2019), with rapid diversification obscuring the signal of extinction. Nevertheless, underestimation of cercopithecoid extinction rates, here and in other studies, is a concern (Rabosky, 2010(Rabosky, , 2016. ...
Objectives: This study examines how speciation and extinction rates vary across primates, with a focus on the recent macroevolutionary dynamics that have shaped extant primate biodiversity.
Materials and methods: Lineage-specific macroevolutionary rates were estimated for each tip in a tree containing 307 species using a hidden-state likelihood model. Differences in tip rates among major clades were evaluated using phylogenetic ANOVA. Differences among diurnal, nocturnal, and cathemeral lineages were also evaluated, based on previous work indicating that activity pattern influences primate diversification.
Results: Rate variation in extant primates is low within clades and high between clades. As in previous studies, cercopithecoids stand out in having high net diversification rates, driven by high speciation rates and very low extinction rates. Platyrrhines combine high speciation and high extinction rates, giving them high rates of lineage turnover. Strepsirrhines and tarsiids have low rates of speciation, extinction, turnover, and net diversification. Hominoids are intermediate between platyrrhines and the strepsirrhine-tarsiid group, and there is evidence for differentiation between hominids and hylobatids. Diurnal lineages have significantly higher speciation rates than nocturnal lineages.
Conclusions: Recent anthropoid macroevolution has been characterized by marked variation in diversification dynamics among clades. Strepsirrhines and tarsiids are more uniform, despite divergent evolutionary and biogeographic histories. Higher speciation rates in diurnal lineages may be driven by greater ecological opportunity or reliance on visual signals for mate recognition. However, the differences among anthropoids indicate that factors other than activity pattern (e.g., clade competition, historical contingency) have had a more influential role in shaping recent primate diversification.
... It is also widely recognised that diversity patterns in the fossil record are skewed by geological and anthropogenic biases 1,6,[30][31][32][33] , fuelling development of increasingly sophisticated methods for quantifying diversification dynamics from incomplete, biased fossil occurrence data. In the last decade, Bayesian approaches, which couple birth-death and preservation processes have enabled estimation of sampling-corrected origination and extinction rates from fossil occurrences [34][35][36][37] , avoiding the problems of inferring these fundamental rates from extant phylogenies [38][39][40][41][42] . In turn, lineage birth and death rates can be modelled as functions of their potential drivers [43][44][45] , permitting separate consideration of the factors that promoted origination or drove extinction. ...
Palaeontologists have long sought to explain the diversification of individual clades to whole biotas at global scales. Advances in our understanding of the spatial distribution of the fossil record through geological time, however, has demonstrated that global trends in biodiversity were a mosaic of regionally heterogeneous diversification processes. Drivers of diversification must presumably have also displayed regional variation to produce the spatial disparities observed in past taxonomic richness. Here, we analyse the fossil record of ammonoids, pelagic shelled cephalopods, through the Late Cretaceous, characterised by some palaeontologists as an interval of biotic decline prior to their total extinction at the Cretaceous-Paleogene boundary. We regionally subdivide this record to eliminate the impacts of spatial sampling biases and infer regional origination and extinction rates corrected for temporal sampling biases using Bayesian methods. We then model these rates using biotic and abiotic drivers commonly inferred to influence diversification. Ammonoid diversification dynamics and responses to this common set of diversity drivers were regionally heterogeneous, do not support ecological decline, and demonstrate that their global diversification signal is influenced by spatial disparities in sampling effort. These results call into question the feasibility of seeking drivers of diversity at global scales in the fossil record.
... As a result, diversification estimates obtained from extant phylogenies alone can provide a biased picture of their dynamics, especially as inferences reach out further into the past. In particular, whether reliable estimates of extinction rate can be obtained from purely extant clades has been questioned (Rabosky 2010). Recent methodological developments have tackled this issue by enabling the integration of information from the fossil record into phylogenetic diversification analyses (Stadler 2010, Heath et al. 2014, Wright et al. 2022. ...
Species diversification—the balance between speciation and extinction—is fundamental to our understanding of how species richness varies in space and time and throughout the Tree of Life. Phylogenetic approaches provide insights into species diversification by enabling support for alternative diversification scenarios to be compared and speciation and extinction rates to be estimated. Here, we review the current toolkit available for conducting such analyses. We first highlight how modeling efforts over the past decade have fostered a notable transition from overly simplistic evolutionary scenarios to a more nuanced understanding of how and why diversification rates vary through time and across lineages. Using the latitudinal diversity gradient as a case study, we then illustrate the impact that modeling choices can have on the results obtained. Finally, we review recent progress in two areas that are still lagging behind: phylogenetic insights into microbial diversification and the speciation process.
... We estimated net diversification rates (speciation minus extinction) with BAMM v.2.5.0 (Rabosky 2014). We did not attempt to separately infer extinction rates, because estimates based on phylogenies largely comprised of extant taxa are frequently unreliable (Rabosky 2010). For analyses, we set the prior expectation for shifts to one, used default Markov Chain Monte Carlo (MCMC) operators, ran MCMC for 2*10 5 generations, and set additional priors using the setBAMMpriors function in the program R v3.4.0 (R Core Team 2017) BAMMtools package ). ...
Migration independently evolved numerous times in animals, with a myriad of ecological and evolutionary implications. In fishes, perhaps the most extreme form of migration is diadromy, the migration between marine and freshwater environments. Key and longstanding questions are: how many times has diadromy evolved in fishes, how frequently do diadromous clades give rise to non-diadromous species, and does diadromy influence lineage diversification rates? Many diadromous fishes have large geographic ranges with constituent populations that use isolated freshwater habitats. This may limit gene flow among some populations, increasing the likelihood of speciation in diadromous lineages relative to non-diadromous lineages. Alternatively, diadromy may reduce lineage diversification rates if migration is associated with enhanced dispersal capacity that facilitates gene flow within and between populations. Clupeiformes (herrings, sardines, shads and anchovies) is a model clade for testing hypotheses about the evolution of diadromy because it includes an exceptionally high proportion of diadromous species and several independent evolutionary origins of diadromy. However, relationships among major clupeiform lineages remain unresolved and existing phylogenies sparsely sampled diadromous species, limiting the resolution of phylogenetically-informed statistical analyses. We assembled a phylogenomic dataset and used multi-species coalescent and concatenation-based approaches to generate the most comprehensive, highly-resolved clupeiform phylogeny to date, clarifying associations among several major clades and identifying recalcitrant relationships needing further examination. We determined that variation in rates of sequence evolution (heterotachy) and base-composition (non-stationarity) had little impact on our results. Using this phylogeny, we characterized evolutionary patterns of diadromy and tested for differences in lineage diversification rates between diadromous, marine, and freshwater lineages. We identified thirteen transitions to diadromy, all during the Cenozoic Era (ten origins of anadromy, two origins of catadromy, and one origin of amphidromy), and seven losses of diadromy. Two diadromous lineages rapidly generated non-diadromous species, demonstrating that diadromy is not an evolutionary dead-end. We discovered considerably faster transition rates out of diadromy than to diadromy. The largest lineage diversification rate increase in Clupeiformes was associated with a transition to diadromy, but we uncovered little statistical support for categorically faster lineage diversification rates in diadromous versus non-diadromous fishes. We propose that diadromy may increase the potential for accelerated lineage diversification, particularly in species that migrate long distances. However, this potential may only be realized in certain biogeographic contexts, such as when diadromy allows access to ecosystems in which there is limited competition from incumbent species.
... Nee et al. [3] demonstrated that extinction rates can be estimated, and mass extinction events can be inferred, from lineage-through-time (LTT) plots that only contain information about lineage "births." Estimation of extinction rates from phylogenies of extant taxa proved controversial: Rabosky [4] went so far as to argue that extinction rates should not even be estimated from molecular phylogenies, while others, such as Beaulieu and O'Meara [5], have argued that reliable extinction estimates can be gleaned from phylogenies that are sufficiently large using sophisticated methods that incorporate things like rate heterogeneity. Most recently, Louca and Pennell [6] demonstrated that speciation and extinction rates cannot be reliably inferred from LTTs derived from time-calibrated trees, inspiring widespread concern about the degree to which inferences from phylogenies are stretched. ...
Last year, a study published in Biology Letters by Thompson and Ramírez-Barahona (2023) argued that, according to analyses of diversification on two massive molecular phylogenies comprising thousands of species, there is no evidence that angiosperms (i.e., flowering plants) were affected by the Cretaceous-Paleogene mass extinction. Here I show that these conclusions are flawed from both methodological and philosophical perspectives. I demonstrate that the methods used in their study possess statistical limitations that strongly reduce the power to detect a true mass extinction event using data similar to those analyzed by Thompson and Ramírez-Barahona (2023). Additionally, I use their study as a springboard to examine the relationship between phylogenetic and fossil evidence in diversification studies.
... The most general limitation is model misspecification (Carruthers and Scotland, 2021); it stems from the fact that all the extinction models used for inference are, as any mathematical model, abstract constructs that will never encompass every detail of real-world processes. Some of the main simplifying assumptions in diversification studies are (1) rates of extinction varying as a (piecewise-)constant or smooth function of time, while in reality the fossil record reveals much more erratic dynamics (see Fig. 3), (2) homogeneous rates among clades, while in reality heterogeneity seems pervasive and can distort extinction rate estimates (Rabosky, 2010, but see Beaulieu and O'Meara, 2015), (3) ideal taxon sampling, while in reality only a fraction of current species is usually sampled, with non-random patterns (Chang et al., 2020) and (4) independence of the process between lineages, while in reality biotic interactions (Aristide and Morlon, 2019) and diversity-dependence (Etienne et al., 2012) are expected to play a significant role on extinction dynamics. Simulation-based evaluations are then crucial to assess the degree to which such misspecifications are expected to alter the precision and accuracy of rate estimates (Carruthers and Scotland, 2021), and, when they cannot be neglected, new model extensions have to be developed to avoid misspecification. ...
... Understanding the patterns and processes that shape the tree of life is one of the central pursuits of biology. However, inferring the tempo of evolution among lineages-the patterns of speciation and extinction that gave rise to our extant biodiversity-remains a difficult problem both theoretically and computationally (Louca & Pennell, 2020;Moore et al., 2016;Rabosky, 2010). ...
Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods are hotly debated. Here we test whether five Bayesian methods—Bayesian Analysis of Macroevolutionary Mixtures (BAMM), two implementations of the Lineage-Specific Birth–Death–Shift model (LSBDS and PESTO), the approximate Multi-Type Birth–Death model (MTBD; implemented in BEAST2), and the Cladogenetic Diversification Rate Shift model (ClaDS2)—produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diversification rates is strongly method dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system.
... It also accounts for extinction via an extinction fraction. Estimating extinction rates without fossil data is controversial [71][72][73] , and the fossil record is poor for most anuran families 74,75 . Thus, we considered various possible extinction fractions and found our results were largely insensitive to fractions ranging from no extinction (ε = 0) to very high (ε = 0.9) extinction ( Supplementary Fig. 3). ...
Most of life’s vast diversity of species and phenotypes is often attributed to adaptive radiation. Yet its contribution to species and phenotypic diversity of a major group has not been examined. Two key questions remain unresolved. First, what proportion of clades show macroevolutionary dynamics similar to adaptive radiations? Second, what proportion of overall species richness and phenotypic diversity do these adaptive-radiation-like clades contain? We address these questions with phylogenetic and morphological data for 1226 frog species across 43 families (which represent >99% of all species). Less than half of frog families resembled adaptive radiations (with rapid diversification and morphological evolution). Yet, these adaptive-radiation-like clades encompassed ~75% of both morphological and species diversity, despite rapid rates in other clades (e.g., non-adaptive radiations). Overall, we support the importance of adaptive-radiation-like evolution for explaining diversity patterns and provide a framework for characterizing macroevolutionary dynamics and diversity patterns in other groups.
... Despite this, these approximations, while overcoming some of the shortcomings of the fossil record, lack several of the important qualities of fossil occurrence data for the study of past diversity (Foote, 1996;Quental and Marshall, 2010). In fact, both types of data have produced several contrasting results regarding key aspects of the evolution of life on Earth, often pointing to the existence of gaps in the fossil record, but also showing the failure of molecular phylogenies to correctly estimate extinction rates (Rabosky, 2010;Puttick et al., 2016). In the last decades, several efforts have allowed the joint analysis of both molecular and morphological data in phylogenetic contexts, showing that these kinds of approaches provide a better picture of the phylogenetic relationships and diversity of clades (Ronquist et al., 2016). ...
... An important caveat to this conclusion is that extinction rates could not be reliably estimated from the phylogenetic tree used in the analysis, with most estimates being close to zero. That the shape of a phylogenetic tree can be used to make inferences about extinction rates has been demonstrated mathematically (Nee et al., 1994), but it has proven to be challenging for many empirical phylogenies, leading some researchers to argue against the approach (Quental and Marshall, 2010;Rabosky, 2010Rabosky, , 2016Louca and Pennell, 2021; but see Morlon, 2014;Beaulieu and O'Meara, 2015). Paleontological data have the potential to offer a more rigorous test for differences in extinction rates, but inferring activity pattern-especially cathemerality-with confidence from fossilizable anatomy is a considerable challenge in mammals (Kay and Kirk, 2000;Smith et al., 2018). ...
Activity pattern has played a prominent role in discussions of primate evolutionary history. Most primates are either diurnal or nocturnal, but a small number are active both diurnally and nocturnally. This pattern—cathemerality—also occurs at low frequency across mammals. Using a large sample of mammalian species, this study evaluates two macroevolutionary hypotheses proposed to explain why cathemerality is less common than diurnality and nocturnality: (1) that cathemeral lineages have higher extinction probabilities (differential diversification), and (2) that transitions out of cathemerality are more frequent, making it a less persistent state (differential state persistence). Rates of speciation, extinction, and transition between character states were estimated using hidden-rates models applied to a phylogenetic tree containing 3013 mammals classified by activity pattern. The models failed to detect consistent differences in diversification dynamics among activity patterns, but there is strong support for differential state persistence. Transition rates out of cathemerality tend to be much higher than transition rates out of nocturnality. Transition rates out of diurnality are similar to those for cathemerality in most clades, with two important exceptions: diurnality is unusually persistent in anthropoid primates and sciurid rodents. These two groups combine very low rates of transition out of diurnality with high speciation rates. This combination has no parallels among cathemeral lineages, explaining why diurnality has become more common than cathemerality in mammals. Similarly, the combination of rates found in anthropoids is sufficient to explain the low relative frequency of cathemerality in primates, making it unnecessary to appeal to high extinction probabilities in cathemeral lineages in this clade. These findings support the hypothesis that the distribution of activity patterns across mammals has been influenced primarily by differential state persistence, whereas the effect of differential diversification appears to have been more idiosyncratic.
... We recover a ~13 Ma gap of no diversification in the cyt-b tree (~ 5 Ma in the nuclear species tree) between the fangless and rear-fanged homalopsids, potentially indicating unsampled extinction events (Ricklefs, 2007). Testing for extinction in future studies will be an interesting investigation into homalopsid evolutionary history but is not possible in our study due to the absence of any known homalopsid fossils (Rabosky, 2010). Since no fossils exist, we had to rely on one fossil and two secondary calibrations for our divergence time estimations. ...
Our knowledge of the biodiversity of Asia and Australasia continues to expand with more focused studies on systematics of various groups and their biogeography. Historically, fluctuating sea levels and cyclic connection and separation of now-disjunct landmasses have been invoked to explain the accumulation of biodiversity via species pump mechanisms. However, recent research has shown that geological shifts of the mainland and species dispersal events may be better explanations of the biodiversity in these regions. We investigate these processes using the poorly studied and geographically widespread Mud Snakes (Serpentes: Homalopsidae) using a target capture approach of ~4,800 nuclear loci from fresh tissues and supplemental mitochondrial data from formalin tissues from museum specimens. We use these datasets to reconstruct the first resolved phylogeny of the group, identify their biogeographic origins, and test hypotheses regarding the roles of sea-level change and habitat selection on their diversification. Divergence dating and ancestral range estimation yielded support for an Oligocene origin and diversification from mainland Southeast Asia and Sundaland in the rear-fanged group ~20 million years ago, followed by eastward and westward dispersal. GeoHiSSE models indicate that niche expansion of ancestral, rear-fanged lineages into aquatic environments did not impact their diversification rates. Our results highlight that Pleistocene sea-level changes and habitat specificity did not primarily lead to the extant species richness of Homalopsidae and that, alternatively, geological shifts in mainland Southeast Asia may have been a major driver of diversity in this group. We also emphasize the importance of using fresh and degraded tissues, and both nuclear and mitochondrial DNA, for filling knowledge gaps in poorly known but highly diverse and conceptually important groups. Here, Homalopsidae represents a non-traditional but effective model study system for understanding transitions between terrestrial, marine, and freshwater environments.
... Any existing estimates of microbial diversification are derived from phylogenetic data (Louca et al., 2018;Scholl & Wiens, 2016). Due to the nearly nonexistent microbial fossil record, these phylogenies are constructed solely from molecular data, which may lead to incorrect rate estimation when diversification rates vary among lineages (Rabosky, 2010;Stadler, 2009). These phylogenies can also be generated by highly dissimilar birth-death processes that have divergent speciation and extinction dynamics (Louca & Pennell, 2020). ...
Biologists have long sought to quantify the number of species on Earth. Often missing from these efforts is the contribution of microorganisms, the smallest but most abundant form of life on the planet. Despite recent large‐scale sampling efforts, estimates of global microbial diversity span many orders of magnitude. It is important to consider how speciation and extinction over the last 4 billion years constrain inventories of biodiversity. We parameterized macroevolutionary models based on birth–death processes that assume constant and universal speciation and extinction rates. The models reveal that richness beyond 10 ¹² species is feasible and in agreement with empirical predictions. Additional simulations suggest that mass extinction events do not place hard limits on modern‐day microbial diversity. Together, our study provides independent support for a massive global‐scale microbiome while shedding light on the upper limits of life on Earth.
... Direct inference from the fossil record can be challenged by gaps in spatial, temporal, and taxonomic coverage. Inferences from molecular phylogenies are similarly fraught: extinction is notoriously difficult to estimate (88,89), and recent work suggests that any given extant timetree can be explained equally well by a large number of diversification scenarios (90). The latter represents a case of nonidentifiability, meaning that it is difficult to infer the true values of a given model's underlying parameters. ...
The latitudinal diversity gradient (LDG) describes the pattern of increasing numbers of species from the poles to the equator. Although recognized for over 200 years, the mechanisms responsible for the largest-scale and longest-known pattern in macroecology are still actively debated. I argue here that any explanation for the LDG must invoke differential rates of speciation, extinction, extirpation, or dispersal. These processes themselves may be governed by numerous abiotic or biotic factors. Hypotheses that claim not to invoke differential rates, such as 'age and area' or 'time for diversification', eschew focus from rate variation that is assumed by these explanations. There is still significant uncertainty in how rates of speciation, extinction, extirpation, and dispersal have varied regionally over Earth history. However, to better understand the development of LDGs, we need to better constrain this variation. Only then will the drivers of such rate variation - be they abiotic or biotic in nature - become clearer.
... Nakov et al., 2018). Since the relative contribution of extinction to the diversification process is unknown or hard to estimate (Rabosky, 2010), net diversification estimates were calculated under two different scenarios of fixed extinction fraction (e): no extinction (e = 0) and high relative extinction (e = 0.9). The reasoning behind our choice of diversification estimator (and possible caveats) can be found in the Methods S3. ...
Climbers germinate on the ground but need external support to sustain their stems, which are maintained attached to supports through modified organs, that is, climbing mechanisms. Specialized climbing mechanisms have been linked to higher diversification rates. Also, different mechanisms may have different support diameter restrictions, which might influence climbers' spatial distribution.
We test these assumptions by linking climbing mechanisms to the spatiotemporal diversification of neotropical climbers. A dataset of climbing mechanisms is presented for 9071 species. WCVP was used to standardize species names, map geographical distributions, and estimate diversification rates of lineages with different mechanisms.
Twiners appear concentrated in the Dry Diagonal of South America and climbers with adhesive roots in the Chocó region and Central America. However, climbing mechanisms do not significantly influence the distribution of neotropical climbers. Also, we found no strong support for correlations between specialized climbing mechanisms and higher diversification rates.
Climbing mechanisms do not strongly impact the spatiotemporal diversification of neotropical climbers on a macroevolutionary scale. We argue that the climbing habit is a synnovation, meaning the spatiotemporal diversification it promotes is due to the sum effect of all the habit's traits rather than isolated traits, such as climbing mechanisms.
... [7]), divergence times [1], and diversification rates (e.g. [8]). ...
Incorporating morphological data into modern phylogenies allows integration of fossil evidence, facilitating divergence dating and macroevolutionary inferences. Improvements in the phylogenetic utility of morphological data have been sought via Procrustes-based geometric morphometrics (GMM), but with mixed success and little clarity over what anatomical areas are most suitable. Here, we assess GMM-based phylogenetic reconstructions in a heavily sampled source of discrete characters for mammalian phylogenetics—the basicranium—in 57 species of marsupial mammals, compared with the remainder of the cranium. We show less phylogenetic signal in the basicranium compared with a ‘Rest of Cranium’ partition, using diverse metrics of phylogenetic signal ( K mult , phylogenetically aligned principal components analysis, comparisons of UPGMA/neighbour-joining/parsimony trees and cophenetic distances to a reference phylogeny) for scaled, Procrustes-aligned landmarks and allometry-corrected residuals. Surprisingly, a similar pattern emerged from parsimony-based analyses of discrete cranial characters. The consistent results across methods suggest that easily computed metrics such as K mult can provide good guidance on phylogenetic information in a landmarking configuration. In addition, GMM data may be less informative for intricate but conservative anatomical regions such as the basicranium, while better—but not necessarily novel—phylogenetic information can be expected for broadly characterized shapes such as entire bones.
This article is part of the theme issue ‘The mammalian skull: development, structure and function’.
... While we cannot exclude these potential errors completely, we accounted for some of the resultant uncertainty by using multiple methods to estimate speciation rates (BAMM, ClaDS, DR) and correlating these estimates with traits and their evolutionary rates using methods that, even though they differ principally in their assumptions and limitations, converged on similar conclusions (Cor-STRATES, PGLS, GLMM, STRAPP, ES-sim) (figure 2). We avoided interpreting the estimates of historical speciation and extinction rates, as these are notoriously hard to reliably tease apart [76] and, instead, focus on present-day estimates royalsocietypublishing.org/journal/rspb Proc. R. Soc. ...
How traits affect speciation is a long-standing question in evolution. We investigate whether speciation rates are affected by the traits themselves or by the rates of their evolution, in hummingbirds, a clade with great variation in speciation rates, morphology and ecological niches. Further, we test two opposing hypotheses, postulating that speciation rates are promoted by trait conservatism or, alternatively, by trait divergence. To address these questions, we analyse morphological (body mass and bill length) and niche traits (temperature and precipitation position and breadth, and mid-elevation), using a variety of methods to estimate speciation rates and correlate them with traits and their evolutionary rates. When it comes to the traits, we find faster speciation in smaller hummingbirds with shorter bills, living at higher elevations and experiencing greater temperature ranges. As for the trait evolutionary rates, we find that speciation increases with rates of divergence in the niche traits, but not in the morphological traits. Together, these results reveal the interplay of mechanisms through which different traits and their evolutionary rates (conservatism or divergence) influence the origination of hummingbird diversity.
... Yet, the ability of a method to estimate speciation and extinction rates should be evaluated with simulations on a method-bymethod basis, not based on sweeping extrapolations from one or a few methods (e.g. Rabosky, 2010;Louca & Pennell, 2020). Furthermore, fluctuations in speciation and extinction rates within clades over time (the focus of Louca & Pennell, 2020) are not the focus here. ...
Understanding the origins of species richness patterns is a fundamental goal in ecology and evolutionary biology. Much research has focused on explaining two kinds of species richness patterns: (i) spatial species richness patterns (e.g. the latitudinal diversity gradient), and (ii) clade-based species richness patterns (e.g. the predominance of angiosperm species among plants). Here, I highlight a third kind of richness pattern: trait-based species richness (e.g. the number of species with each state of a character, such as diet or body size). Trait-based richness patterns are relevant to many topics in ecology and evolution, from ecosystem function to adaptive radiation to the paradox of sex. Although many studies have described particular trait-based richness patterns, the origins of these patterns remain far less understood, and trait-based richness has not been emphasised as a general category of richness patterns. Here, I describe a conceptual framework for how trait-based richness patterns arise compared to other richness patterns. A systematic review suggests that trait-based richness patterns are most often explained by when each state originates within a group (i.e. older states generally have higher richness), and not by differences in transition rates among states or faster diversification of species with certain states. This latter result contrasts with the widespread emphasis on diversification rates in species-richness research. I show that many recent studies of spatial richness patterns are actually studies of trait-based richness patterns, potentially confounding the causes of these patterns. Finally, I describe a plethora of unanswered questions related to trait-based richness patterns.
... However, extinction rate remained stable and almost null throughout the evolutionary history of the group (Fig. 4.2D). In the absence of a fossil record, molecular phylogenies including only extant species are known to produce unrealistically low estimates of extinction rate (see Quental and Marshall, 2010;Rabosky, 2010;Stadler, 2013;Silvestro et al., 2018). Although our results were found to be concordant amongst the different methods, some of which have been used to obtain estimates that are more consistent with the fossil record (Morlon et al., 2010(Morlon et al., , 2011, we preferred to focus our interpretation of macroevolutionary rates variation through time on speciation rate. ...
... The mean and median estimates for 2 µ were however fairly estimated. Poor extinction rate parameter estimates may be due to the fact that generally the extinction (death) rate parameters are poorly estimated by general constant birth-death models[29] [30][31]. When the probability of re-H. ...
... Although it has been shown that species with broader ranges tend to have both lower extinction risk and also lower speciation rates (Purvis et al. 2000;Greenberg & Mooers 2017), we found that open nesting species (with either small or wide niches/ranges) tend to have lower extinction rates compared to species with domed nests. We, however, strongly highlight that estimates of extinction rates from molecular phylogenies should be taken with extreme caution (Rabosky 2010) and differences in rates were smaller when the dataset used included only species with genetic data. In any case, our results do not support the hypothesis of higher speciation rates in species with open nests, and instead show that high speciation rates are mostly related to small range sizes, supporting previous findings (Cally et al. 2021). ...
Bird nests are essential structures that directly determine the fitness of an organism. While there is theory and evidence predicting an association between species nest traits and their habitat, few studies have comprehensively examined the macroevolutionary patterns driving nest evolution, species niche and their interrelation. Using information on 3174 species of songbirds, we show that species that build domed nests (i.e. nests with a roof) have smaller ranges, narrower thermal niches, are less likely to colonise urban environments and have potentially higher extinction rates compared to species that build open nests. Moreover, we show that these macroevolutionary patterns could be driven by the higher energetic demands when building domed nests, which consumes more time and might restrict breeding opportunities. These diverse strands of evidence suggest that the transition from domed to open nests in passerines represents an important evolutionary innovation behind the success of the largest radiation of birds.
... third scenario) seems unlikely according to our results, as we found no differences in extinction rates between the two main lineages. However, this possibility cannot be ruled out considering the ongoing discussion about what can be inferred about past diversification processes from extant timetrees alone, including the caveats of estimating extinction rates from molecular phylogenies in the absence of fossil data (Louca & Pennell, 2021;Rabosky, 2010), and the identifiability of alternative speciation and extinction parameters (Louca & Pennell, 2020, but see Morlon et al., 2022). Unfortunately, most fossil records of akodontines correspond to living species (Pardiñas et al., 2002) and the few records of certainly extinct species are difficult to place phylogenetically, owing to the fragmentary state of the material (Pardiñas et al., 2002), limiting their use in assessing this scenario. ...
A link between morphological diversity and species richness is often implied in several evolutionary concepts, but conflicting results hamper a more direct link between these variables. Using a morphologically and ecologically diverse clade of Neotropical cricetids, Akodontini, we (1) characterized the tribe’s patterns of morphological disparity and lineage diversification, contrasting the two major clades; and (2) tested whether morphological disparity and rates of morphological evolution are associated with their lineage diversification patterns. We found no correlation between diversification rates and morphological patterns; instead, our results reveal a pattern of ecological and morphological diversification that is independent of cladogenetic events. We found higher rates of morphological evolution in lineages with longer independent evolutionary histories, leading to fewer, but more disparate and specialized species occupying the peripheral areas of the ecomorphospace and increasing the overall morphological diversity of the group.
... Our trait independent analyses on diversification found strong evidence for rate homogeneity in speciation rates across diplodactyloids. We note that there is little information content in molecular phylogenies in terms of underlying diversification processes and that numerous patterns can lead to signatures of decline in diversification rate (Louca & Pennell, 2019;Quental & Marshall, 2010, 2011Rabosky, 2010Rabosky, , 2016. Further, we do not argue that the absolute estimates of r, λ, and μ represent biological reality given the issues of relying on such approximations. ...
A key area of interest in evolutionary biology has been understanding the role of ecological opportunity in the formation of adaptive radiations, lineages where speciation and phenotypic diversification are driven by open ecological opportunity. Evolutionary theory posits that adaptive radiations should show initial bursts of ecomorphological diversification and rapid speciation, and that these two processes are correlated. Here, we investigate and contrast these predictions across ecomorphologically diverse continental (Australia) and insular (New Caledonia and New Zealand) radiations of diplodactyloid geckos. We test two key hypotheses: (a) that island colonization and the transition to novel niche-space has resulted in increased rates of speciation and trait diversification and (b) that rates of morphological diversification are correlated across multiple trait axes. Surprisingly, we find that speciation rate is homogenous and morphological diversification rates are idiosyncratic and uncorrelated with speciation rates. Tests of morphological integration suggests that while all traits coevolve, constraint may act differentially on individual axes. This accords with a growing number of studies indicating that ecologically diverse and species-rich radiations can show limited or no evidence of exceptional regime shifts in speciation dynamics or morphological diversification, especially in continental contexts.
... Although new methodologies have been developed to take into account time, diversity, and trait dependences on speciation rates (FitzJohn, 2010;Pyron and Burbrink, 2013;Herrera-Alsina et al., 2019), these approaches are still limited by the availability of data on extinct and extant taxa. Moreover, speciation rates are inextricably connected to extinction rates and estimation of the latter is challenging, particularly in cases where there is no fossil data of now extinct species to inform methods (Rabosky, 2010). Recent work has also suggested that the inference models for speciation and extinction rates present intrinsic methodological limitations, leading to infinite indistinguishable diversification scenarios of speciation rates for the same time-calibrated phylogenies (Louca and Pennell, 2020). ...
A bstract
The total number of species on earth and the rate at which new species are created are fundamental questions for ecology, evolution and conservation. These questions have typically been approached separately, despite their obvious interconnection. In this manuscript we approach both questions in conjunction, for all terrestrial animals, which enables a more holistic integration and generates novel emergent predictions. To do this, we combine two previously unconnected bodies of theory: general ecosystem modelling and individual based ecological neutral theory. General ecosystem models provide us with estimated numbers of individual organisms, separated by functional group and body size. Neutral theory, applied within a guild of functionally similar individuals, connects species richness, speciation rate and number of individual organisms. In combination, for terrestrial endotherms where species numbers are known, they provide us with estimates for speciation rates as a function of body size and diet class. Extrapolating the same rates to guilds of ectotherms enables us to estimate the species richness of those groups, including species yet to be described. We find that speciation rates per species per million years decrease with increasing body size. Rates are also higher for carnivores compared to omnivores or herbivores of the same body size. Our estimate for the total number of terrestrial species of animals is in the range 1.03 − 2.92 million species, a value consistent with estimates from previous studies, despite having used a fundamentally new approach. Perhaps what is most remarkable about these results is that they have been obtained using only limited data from larger endotherms and their speciation rates, with the rest of the predictive process being based on mechanistic theory. This work illustrates the potential of a new approach to classic eco-evolutionary questions, while also adding weight to existing predictions. As we now face an era of dramatic biological change, new methods will be needed to mechanistically model global biodiversity at the species and individual organism level. This will be a huge challenge but the combination of general ecosystem models and neutral theory that we introduce here could be the only way to tractably achieve it.
... The extinction rate remained stable and almost null throughout the evolutionary history of the group (Supplementary Fig. S13). In the absence of a fossil record, molecular phylogenies including only extant species are known to produce unrealistically low estimates of extinction rate (see Quental and Marshall, 2010;Rabosky, 2010;Stadler, 2013;Silvestro et al., 2018;Louca and Pennell, 2021). The analyses we performed with ACDC suggested that alternative extinction rate scenarios of higher rate magnitudes and with mostly constant or increasing trends towards the present might be part of the set of congruent models of our diversification hypothesis given, however, the same temporal trend and magnitude in netdiversification rate . ...
Most of the unique and diverse vertebrate fauna that inhabits Madagascar derives from in situ diversification from colonisers that reached this continental island through overseas dispersal. The endemic Malagasy Scincinae lizards are amongst the most species-rich squamate groups on the island. They colonised all bioclimatic zones and display many ecomorphological adaptations to a fossorial (burrowing) lifestyle. Here we propose a new phylogenetic hypothesis for their diversification based on the largest taxon sampling so far compiled for this group. We estimated divergence times and investigated several aspects of their diversification (diversification rate, body size and fossorial lifestyle evolution, and biogeography). We found that diversification rate was constant throughout most of the evolutionary history of the group, but decreased over the last 6–4 million years and independently from body size and fossorial lifestyle evolution. Fossoriality has evolved from fully quadrupedal ancestors at least five times independently, which demonstrates that even complex morphological syndromes – in this case involving traits such as limb regression, body elongation, modification of cephalic scalation, depigmentation, and eyes and ear-opening regression – can evolve repeatedly and independently given enough time and eco-evolutionary advantages. Initial diversification of the group likely occurred in forests, and the divergence of sand-swimmer genera around 20 Ma appears linked to a period of aridification. Our results show that the large phenotypic variability of Malagasy Scincinae has not influenced diversification rate and that their rich species diversity results from a constant accumulation of lineages through time. By compiling large geographic and trait-related datasets together with the computation of a new time tree for the group, our study contributes important insights on the diversification of Malagasy vertebrates.
... The posterior distribution of extinction rate (m) overlapped zero ( Figure S4), suggesting that extinction has not been high in Hydromyini, or is not recoverable from molecular data. 42 For the Pseudomys Division, the best model was one where speciation increased exponentially with time ( Figure 2A). For all other divisions within the Sahul Hydromyini, the best fitting diversification model was one with constant speciation and extinction ( Figure 2B; Table S2). ...
Sahul unites the world’s largest and highest tropical island and the oldest and most arid continent on the backdrop of dynamic environmental conditions. Massive geological uplift in New Guinea is predicted to have acted as a species pump from the late Miocene onward, but the impact of this process on biogeography and diversification remains untested across Sahul as a whole. To address this, we reconstruct the assembly of a recent and diverse radiation of rodents (Murinae: Hydromyini) spanning New Guinea, Australia, and oceanic islands. Using phylogenomic data from 270 specimens, including many recently extinct and highly elusive species, we find that the orogeny and expansion of New Guinea opened ecological opportunity and triggered diversification across a continent. After a single over-water colonization from Asia ca. 8.5 Ma, ancestral Hydromyini were restricted to the tropical rainforest of proto-New Guinea for 3.5 million years. Following a shift in diversification coincident with the orogeny of New Guinea ca. 5 Ma and subsequent colonization of Australia, transitions between geographic regions (n = 24) and biomes (n = 34) become frequent. Recurrent over-water colonization between mainland and islands demonstrate how islands can play a substantial role in the assembly of continental fauna. Our results are consistent with a model of increased ecological opportunity across Sahul following major geological uplift in New Guinea ca. 5 Ma, with sustained diversification facilitated by over-water colonization from the Pleistocene to present. We show how geological processes, biome transitions, and over-water colonization collectively drove the diversification of an expansive continental radiation.
The evolutionary histories of major clades, including mammals, often comprise changes in their diversification dynamics, but how these changes occur remains debated. We combined comprehensive phylogenetic and fossil information in a new “birth-death diffusion” model that provides a detailed characterization of variation in diversification rates in mammals. We found an early rising and sustained diversification scenario, wherein speciation rates increased before and during the Cretaceous-Paleogene (K-Pg) boundary. The K-Pg mass extinction event filtered out more slowly speciating lineages and was followed by a subsequent slowing in speciation rates rather than rebounds. These dynamics arose from an imbalanced speciation process, with separate lineages giving rise to many, less speciation-prone descendants. Diversity seems to have been brought about by these isolated, fast-speciating lineages, rather than by a few punctuated innovations.
Colonization of a novel geographic area is a classic source of ecological opportunity. Likewise, complex microhabitats are thought to promote biodiversity. We sought to reconcile these two predictions when they are naturally opposing outcomes. We assess the macroevolutionary consequences of an ancestral shift from benthic to pelagic microhabitat zones on rates of speciation and phenotypic evolution in North American minnows. Pelagic species have more similar phenotypes and slower rates of phenotypic evolution, but faster speciation rates, than benthic species. These are likely two independent, opposing responses to specialization along the benthic-pelagic axis, as rates of phenotypic evolution and speciation are not directly correlated. The pelagic zone is more structurally homogenous and offers less ecological opportunity, acting as an ecological dead end for minnows. In contrast, pelagic species may be more mobile and prone to dispersal and subsequent geographic isolation and, consequently, experience elevated instances of allopatric speciation. Microhabitat shifts can have decoupled effects on different dimensions of biodiversity, highlighting the need for nuance when interpreting the macroevolutionary consequences of ecological opportunity.
It is standard statistical practice to provide measures of uncertainty around parameter estimates. Unfortunately, this very basic and necessary enterprise is often absent in macroevolutionary studies using maximum likelihood estimates (MLEs).
dentist is an R package that allows an approximation of confidence intervals (CI) around parameter estimates without an analytic solution to likelihood equations. This package works by ‘denting’ the likelihood surface by sampling points a specified distance around the MLE following what is essentially a Metropolis‐Hastings walk.
We describe the importance of estimating uncertainty around parameter estimates, as well as demonstrate the ability of dentist to accurately approximate CI.
We introduce several plotting tools to visualize the results of a dentist analysis. dentist is freely available from https://github.com/bomeara/dentist , written in the R language, and can be used for any given likelihood function.
Snakes and lizards (Squamata) represent a third of terrestrial vertebrates and exhibit spectacular innovations in locomotion, feeding, and sensory processing. However, the evolutionary drivers of this radiation remain poorly known. We infer potential causes and ultimate consequences of squamate macroevolution by combining individual-based natural history observations (>60,000 animals) with a comprehensive time-calibrated phylogeny that we anchored with genomic data (5400 loci) from 1018 species. Due to shifts in the dynamics of speciation and phenotypic evolution, snakes have transformed the trophic structure of animal communities through the recurrent origin and diversification of specialized predatory strategies. Squamate biodiversity reflects a legacy of singular events that occurred during the early history of snakes and reveals the impact of historical contingency on vertebrate biodiversity.
Aim. Species age, the elapsed time since origination, can give an insight into how species longevity might influence eco-evolutionary dynamics and has been hypothesized to influence extinction risk. Traditionally, species ages have been measured in the fossil record. However, recently, numerous studies have attempted to estimate the ages of extant species from the branch lengths of time-calibrated phylogenies. This approach poses problems because phylogenetic trees contain direct information about species identity only at the tips and not along the branches. Here, we show that taxon sampling, extinction, and different assumptions about speciation modes can significantly alter the relationship between true species age and phylogenetic branch lengths, leading to high error rates. We find that these biases can lead to erroneous interpretations of eco-evolutionary patterns derived from the comparison between phylogenetic age and other traits, such as extinction risk.
Innovation. For bifurcating speciation, which is the default assumption in most analyses, we propose a probabilistic approach to improve the estimation of species ages, based on the properties of a birth-death process. We show that our model can reduce the error by one order of magnitude under cases of high extinction.
Main conclusion. Our results call for caution in interpreting the relationship between phylogenetic ages and eco-evolutionary traits, and show that, under some assumptions, it is possible to obtain better approximations of species age by combining information from branch lengths with the expectations of a birth-death process.
The extreme asymmetry of species richness distribution across the tree of life has always intrigued evolutionary biologists. Two competing explanations have been proposed to explain this pattern—the clade age hypothesis and diversification rate variation. While these two scenarios may not be mutually exclusive, to what extent time and diversification rates interact to explain species richness patterns remains understudied. Here, we investigate the relative influence of these two scenarios using tarantulas (Family: Theraphosidae) as a model. Tarantulas represent a speciose group of spiders found worldwide but exceptionally diverse in South America. These spiders show two distinct patterns of microhabitat use (ground-dwelling or arboreal) and defense strategies (presence or absence of urticating hairs). Using various trait-independent and dependent diversification models, we test the clade age hypothesis, the role of microhabitat, antipredator defense strategy, and geography in influencing diversification rates. Our results suggest that clade age is the primary predictor of species richness distribution across the tarantula subfamilies. However, the presence of urticating hair probably disrupted this pattern in some clades by increasing the net diversification rates, not by increasing the speciation rate but by reducing the extinction rate.
Understanding palaeodiversity dynamics through time and space is a central goal of macroevolution. Estimating palaeodiversity dynamics has been historically addressed with fossil data because it directly reflects the past variations of biodiversity. Unfortunately, some groups or regions lack a good fossil record, and dated phylogenies can be useful to estimate diversification dynamics. Recent methodological developments have unlocked the possibility to investigate palaeodiversity dynamics by using phylogenetic birth‐death models with non‐homogeneous rates through time and across clades. One of them seems particularly promising to detect clades whose diversity has declined through time. However, empirical applications of the method have been hampered by the lack of a robust, accessible implementation of the whole procedure, therefore requiring users to conduct all the steps of the analysis by hand in a time‐consuming and error‐prone way.
Here we propose an automation of Morlon et al. (2011) clade‐shift model with additional features accounting for recent developments, and we implement it in the R package RPANDA. We also test the approach with simulations focusing on its ability to detect shifts of diversification and to infer palaeodiversity dynamics. Finally, we illustrate the automation by investigating the palaeodiversity dynamics of Cetacea, Vangidae, Parnassiinae and Cycadales.
Simulations showed that we accurately detected shifts of diversification although false shift detections were higher for time‐dependent diversification models with extinction. The median global error of palaeodiversity dynamics estimated with the automated model is low, showing that the method can capture diversity declines. We detected shifts of diversification for three of the four empirical examples considered (Cetacea, Parnassiinae and Cycadales). Our analyses unveil a waxing‐and‐waning pattern due to a phase of negative net diversification rate embedded in the trees after isolating recent radiations.
Our work makes it possible to easily apply non‐homogeneous models of diversification in which rates can vary through time and across clades to reconstruct palaeodiversity dynamics. By doing so, we detected palaeodiversity declines among three of the four groups tested, highlighting that such periods of negative net diversification might be common. We discuss the extent to which this approach might provide reliable estimates of extinction rates, and we provide guidelines for users.
Speciation rates vary greatly among taxa and regions and are shaped by both biotic and abiotic factors. However, the relative importance and interactions of these factors are not well understood. Here we investigate the potential drivers of speciation rates in South American freshwater fishes, the most diverse continental vertebrate fauna, by examining the roles of multiple biotic and abiotic factors. We integrate a dataset on species geographic distribution, phylogenetic, morphological, climatic, and habitat data. We find that Late Neogene-Quaternary speciation events are strongly associated with body-size evolution, particularly in lineages with small body sizes that inhabit higher elevations near the continental periphery. Conversely, the effects of temperature, area, and diversity-dependence, often thought to facilitate speciation, are negligible. By evaluating multiple factors simultaneously, we demonstrate that habitat characteristics associated with elevation, as well as body size evolution, correlate with rapid speciation in South American freshwater fishes. Our study emphasizes the importance of integrative approaches that consider the interplay of biotic and abiotic factors in generating macroecological patterns of species diversity.
Tropical lands harbour the highest number of species, resulting in the ubiquitous latitudinal diversity gradient (LDG). However, exceptions to this pattern have been observed in some taxa, explained by the interaction between the evolutionary histories and environmental factors that constrain species' physiological and ecological requirements. Here, we applied a deconstruction approach to map the detailed species richness patterns of Actinopterygian freshwater fishes at the class and order levels and to disentangle their drivers using geographical ranges and a phylogeny, comprising 77% (12 557) of all described species. We jointly evaluated seven evolutionary and ecological hypotheses posited to explain the LDG: diversification rate, time for speciation, species–area relationship, environmental heterogeneity, energy, temperature seasonality and past temperature stability. We found distinct diversity gradients across orders, including expected, bimodal and inverse LDGs. Despite these differences, the positive effect of evolutionary time explained patterns for all orders, where species-rich regions are inhabited by older species compared to species-poor regions. Overall, the LDG of each order has been shaped by a unique combination of factors, highlighting the importance of performing a joint evaluation of evolutionary, historical and ecological factors at different taxonomic levels to reach a comprehensive understanding on the causes driving global species richness patterns.
Aim
Shifts in diversification rates of Australian flora and fauna have been associated with aridification, but the relationship between diversification rates and aridity has never been quantified. We employed multiple approaches to reconstruct paleoenvironments of Australia for the first time. We used this information, and phylogenetic‐based analyses, to explore how changes in temperature and increasing aridity during the Neogene influenced the diversification of the Australian blindsnakes. We tested whether diversification rates differ between arid‐adapted and mesic‐adapted lineages.
Taxon
Typhlopidae, Anilios blindsnakes.
Location
Australia.
Materials and Methods
We estimated the historical biogeography of blindsnakes using BioGeoBEARS. We synthesised multiple approaches to reconstruct paleotemperature and paleoaridity of Australia during the Neogene. We fitted several birth‐death models and estimated diversification rates under paleoenvironmental conditions using RPANDA. We further compared diversification rates between arid‐adapted lineages versus mesic‐adapted lineages using ClaDS and GeoHiSSE.
Results
Ancestral area estimation indicated Australian blindsnakes have tropical grassland origins. We found that Australia‐specific regional paleotemperature and paleoaridity provided a better explanation for diversification rate variation than global paleotemperature. Specifically, our best‐fitting model indicated that speciation rates of blindsnakes decreased with increasing aridity. We found no difference in diversification rates between arid‐ and mesic‐adapted lineages.
Main Conclusions
Soon after dispersing to Australia, the common ancestors of Australian blindsnakes diversified rapidly in mesic habitats during the early Miocene. However, as the continent became increasingly arid, diversification rates decreased. We found that shifts in the environment led to the emergence of two major clades: one remaining in primarily mesic habitats and the other adapting to the expanding arid biome. Our results emphasise the importance of both arid and tropical biomes as sources and sinks of diversification.
Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods is hotly debated. Here we test whether five Bayesian methods—Bayesian Analysis of Macroevolutionary Mixtures ( BAMM ), two implementations of the Lineage-Specific Birth-Death-Shift model ( LSBDS and PESTO ), the approximate Multi-Type Birth-Death model ( MTBD ; implemented in BEAST2 ), and the cladogenetic diversification rate shift model ( CLaDS2 )—produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diver-sification rates is strongly method-dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system.
Lay Summary
Understanding why some groups of organisms have more species than others is key to understanding the origin of biodiversity. Theory and empirical evidence suggest that multiple distinct historical events—such as the evolution of particular morphological features (e.g., the flower, the tetrapod limb) and competition amongst species—can produce this pattern of divergent species richness. Identifying when and where on the tree of life shifts in diversification rates occur is important for explaining the origin of modern-day biodiversity and understanding how disparity among species evolves. Several statistical methods have been developed to infer diversification rates and identify these shifts. While these methods each attempt to make inferences about changes in the tempo of diversification, they differ in their underlying statistical models and assumptions. Here we test if these methods draw similar conclusions using a dataset of 65 time-calibrated phylogenies from across multicellular life. We find that inferences of where rate shifts occur strongly depends on the chosen method. Therefore, biologists should choose the model whose assumptions they believe to be the most valid and justify their model choice a priori , or consider using several independent methods to test an evolutionary hypothesis.
Recent theoretical work on phylogenetic birth-death models offers differing viewpoints on whether they can be estimated using lineage-through-time data. Louca and Pennell (2020) showed that the class of models with continuously differentiable rate functions is nonidentifiable: any such model is consistent with an infinite collection of alternative models, which are statistically indistinguishable regardless of how much data are collected. Legried and Terhorst (2022) qualified this grave result by showing that identifiability is restored if only piecewise constant rate functions are considered. Here, we contribute new theoretical results to this discussion, in both the positive and negative directions. Our main result is to prove that models based on piecewise polynomial rate functions of any order and with any (finite) number of pieces are statistically identifiable. In particular, this implies that spline-based models with an arbitrary number of knots are identifiable. The proof is simple and self-contained, relying mainly on basic algebra. We complement this positive result with a negative one, which shows that even when identifiability holds, rate function estimation is still a difficult problem. To illustrate this, we prove some rates-of-convergence results for hypothesis testing using birth-death models. These results are information-theoretic lower bounds which apply to all potential estimators.
Reconstructing the biogeographical history and timing of the diversification of temperate forests is essential for understanding their history and resolving uncertainties about how flowering plants emerged from their deep tropical origins to dominate in today's freezing terrestrial environments. The angiosperm order Fagales, comprising iconic components of temperate forests worldwide with an extensive fossil record, are an excellent plant system in which to apply a fossil-aware paradigm, such as the fossilized birth-death (FBD) process, for investigating the macroevolution of temperate forest biomes. Here, we improve upon previous efforts to resolve phylogeny and incorporate fossils in Fagales using low-copy nuclear loci and an expanded morphological matrix to reevaluate the Fagales fossil record and: (1) infer the phylogenetic relationships and the time of origin of the clade using the FBD model as implemented in RevBayes, (2) provide a framework for evaluating the climatic and biogeographic history of Fagales, and (3) investigate how the inclusion of fossils via the FBD method influences ancestral reconstruction and diversification estimation. The phylogenetic relationships we recovered are conventional except for the position of Nothofagaceae, while our inferred ages support older timelines than previously proposed, with a mid-Cretaceous date for the most recent common ancestor of the order. Biogeographical analysis shows an origin of Fagales consistent with an ancestral circumboreal temperate distribution corroborated by ancestral niche reconstructions. While distributions today largely reflect the general conservatism of temperate forests, we identified two episodes of high diversification, one at the mid-Cretaceous origin of the clade and the other continuing from the Miocene to the present. Removing fossil taxa from the tree reveals a different story, shifting the origin of extant families from North America to East Asia, reflecting refugial distributions in this biodiversity "museum" and implying a general bias towards low extinction areas in biogeographic reconstruction. Likewise, without fossil data, diversification estimates were higher and unable to detect an early diversification burst. Based on our analyses, we close with recommendations regarding the interpretation of estimates of diversification and ancestral state reconstruction using phylogenetic trees with only extant species as tips.
Early natural historians-Comte de Buffon, von Humboldt, and De Candolle-established environment and geography as two principal axes determining the distribution of groups of organisms, laying the foundations for biogeography over the subsequent 200 years, yet the relative importance of these two axes remains unresolved. Leveraging phylogenomic and global species distribution data for Mimosoid legumes, a pantropical plant clade of c. 3500 species, we show that the water availability gradient from deserts to rain forests dictates turnover of lineages within continents across the tropics. We demonstrate that 95% of speciation occurs within a precipitation niche, showing profound phylogenetic niche conservatism, and that lineage turnover boundaries coincide with isohyets of precipitation. We reveal similar patterns on different continents, implying that evolution and dispersal follow universal processes.
1. dentist is an R-package that "dents" the likelihood surface by sampling points a specified distance around the maximum likelihood estimate. This allows an estimate of confidence intervals around parameter estimates without an analytic solution to likelihood equations or an approximation based on local curvature at a peak.
2. We describe the importance of estimating uncertainty around parameter estimates as well as demonstrate the ability of dentist to accurately estimate confidence intervals. We introduce several plotting tools to visualize the results of a dentist analysis.
3. dentist is freely available from https://github.com/bomeara/dentist, written in the R language, and can be used for any given likelihood function.
Many of Madagascar’s unique species are threatened with extinction. However, the severity of recent and potential extinctions in a global evolutionary context is unquantified. Here, we compile a phylogenetic dataset for the complete non-marine mammalian biota of Madagascar and estimate natural rates of extinction, colonization, and speciation. We measure how long it would take to restore Madagascar’s mammalian biodiversity under these rates, the “evolutionary return time” (ERT). At the time of human arrival there were approximately 250 species of mammals on Madagascar, resulting from 33 colonisation events (28 by bats), but at least 30 of these species have gone extinct since then. We show that the loss of currently threatened species would have a much deeper long-term impact than all the extinctions since human arrival. A return from current to pre-human diversity would take 1.6 million years (Myr) for bats, and 2.9 Myr for non-volant mammals. However, if species currently classified as threatened go extinct, the ERT rises to 2.9 Myr for bats and 23 Myr for non-volant mammals. Our results suggest that an extinction wave with deep evolutionary impact is imminent on Madagascar unless immediate conservation actions are taken.
White‐eyes are an iconic avian radiation of small passerines that are mainly distributed across the Eastern Hemisphere tropics and subtropics. Species diversity of white‐eyes is particularly high on oceanic islands, and many species are restricted to single islands or island groups. The high rate of species diversification of white‐eyes ranks them among the fastest radiations known in birds, but whether their accelerated diversification was the result of repeatedly colonizing islands remains unexplored. We used a newly estimated timetree for nearly all zosteropids and phylogenetic comparative methods to estimate and compare diversification rates between island and continental lineages. We show that island white‐eyes have similar extinction rates, yet higher speciation rates compared to continental white‐eyes. In addition, we find higher rates of transitions from islands to continents. Our results show the importance of islands, such as Wallacean and Melanesian archipelagos of the Indo‐Pacific, in facilitating high rates of speciation within this remarkable clade.
Premise:
Approximately 14% of all fern species have physiologically active chlorophyllous spores that are much more short-lived than the more common and dormant achlorophyllous spores. Most chlorophyllous-spored species (70%) are epiphytes, and these account for almost 37% of all epiphytic ferns. Chlorophyllous-spored ferns are also overrepresented among species in habitats with waterlogged soils, of which nearly 60% have chlorophyllous spores. Ferns in these disparate habitat types are also united by a low incidence of mycorrhizal associations. We therefore hypothesize that autotrophic chlorophyllous spores represent an adaptation of ferns to habitats with scarce mycorrhizal associations.
Methods:
We evaluated the co-evolution of chlorophyllous spores and mycorrhizal associations in ferns and their relation to habitat type using phylogenetic comparative methods.
Key results:
Although we did not find support for the co-evolution of the spore type and the mycorrhizal associations, we did find that chlorophyllous spores and the absence of mycorrhizal associations have co-evolved with epiphytic and waterlogged habitats. Transition rates to epiphytic and waterlogged habitats were significantly higher in species with chlorophyllous spores compared to achlorophyllous lineages.
Conclusions:
Spore type and mycorrhizal associations appear to play important roles in the radiation of ferns into different habitat types. Future work should focus on clarifying the functional significance of these associations. This article is protected by copyright. All rights reserved.
Studying the relationship between diversification and functional trait evolution among broadly co‐occurring clades can shed light on interactions between ecology and evolutionary history. However, evidence from many studies is compromised because of their focus on overly broad geographic or narrow phylogenetic scales. We addressed these limitations by studying 46 independent, biogeographically delimited clades of songbirds that dispersed from the Eastern Hemisphere into the Americas and assessed (1) whether diversification has varied through time and/or among clades within this assemblage, (2) the extent of heterogeneity in clade‐specific morphological trait disparity and (3) whether morphological disparity among these clades is consistent with a uniform diversification model. We found equivalent support for constant rates birth–death and density‐dependent speciation processes, with notable outliers having significantly fewer or more species than expected given their age. We also found substantial variation in morphological disparity among these clades, but that variation was broadly consistent with uniform evolutionary rates, despite the existence of diversification outliers. These findings indicate relatively continuous, ongoing morphological diversification, arguing against conceptual models of adaptive radiation in these continental clades. Additionally, they suggest surprisingly consistent diversification among the majority of these clades, despite tremendous variance in colonization history, habitat valences and trophic specializations that exist among continental clades of birds. Diversification trends vary between songbird clades in the Americas, but morphological evolution appears surprisingly uniform.
Inferences about macroevolutionary process have traditionally depended solely on the fossil record, but such inferences can be strengthened by also considering the shapes of the phylogenetic trees that link extant taxa. The realization that phylogenies reflect macroevolutionary processes has fed to a growing literature of theoretical and comparative studies of tree shape. Two aspects of tree shape are particularly important: tree balance and the distribution of branch lengths. We examine and evaluate recent developments in and connections between these two aspects, and suggest directions for future research. Studies of tree shape promise useful and powerful tests of macroevolutionary hypotheses. With appropriate further research, tree shape may help us detect mass extinctions and adaptive radiations, measure continuous variation in speciation and extinction rates, and associate changes in these rates with ecological or biogeographical causes. The usefulness of tree shape extends well beyond the study of macroevolution. We discuss applications to other areas of biology, including coevolution, phylogenetic inference, population biology, and developmental biology.
Species extinction is both a key process throughout the history of life and a pressing concern in the conservation of present-day biodiversity. These two facets have largely been studied by separate communities using different approaches. This article illustrates with examples some of the ways that considering the evolutionary relationships among species—phylogenies—has helped the study of both past and present species extinction. The focus is on three topics: extinction rates and severities, phylogenetic nonrandomness of extinction, and the testing of hypotheses relating extinction-proneness to attributes of organisms or species. Phylogenetic and taxic approaches to extinction have not fully fused, largely because of the difficulties of relating discrete taxa to the underlying continuity of phylogeny. Phylogeny must be considered in comparative tests of hypotheses about extinction, but care must be taken to avoid overcorrecting for phylogenetic nonindependence among taxa.
Although they typically do not provide reliable information on divergence times, supertrees are nevertheless attractive candidates for the study of diversification rates: by combining a collection of less inclusive source trees, they promise to increase both the number and density of taxa included in the composite phylogeny. The relatively large size and possibly more dense taxonomic sampling of supertrees have the potential to increase the statistical power and decrease the bias, respectively, of methods for studying diversification rates that are robust to uncertainty regarding the timing of diversification events. These considerations motivate the development of atemporal methods that can take advantage of recent and anticipated advances in supertree estimation. Herein, we describe a set of whole-tree, topology- based methods intended to address two questions pertaining to the study of diversification rates. First, has a given (super)tree experienced significant variation in diversification rates among its branches? Second, if so, where have significant shifts in diversification rate occurred? We present results of simulation studies that characterize the statistical behavior of these methods, illustrating their increased power and decreased bias. We also applied the methods to a published supertree of primates, demonstrating their ability to contend with relatively large, incompletely resolved (super)trees. All the methods described in this chapter have been implemented in the freely available program, SYMMETREE.
Honing Bivalve History
What are the lasting effects of extinction, both persistent background extinctions and major events, on surviving lineages? Roy et al. (p. 733 ) examined the excellent fossil record of marine bivalves over the past 200 million years, which spans the end-Cretaceous extinction. Background extinctions tended to be higher within certain lineages and depended on the previous history of extinctions within those lineages. Cenozoic taxa are still reflecting the end-Cretaceous event.
The uneven distribution of species richness is a fundamental and unexplained pattern of vertebrate biodiversity. Although species richness in groups like mammals, birds, or teleost fishes is often attributed to accelerated cladogenesis, we lack a quantitative conceptual framework for identifying and comparing the exceptional changes of tempo in vertebrate evolutionary history. We develop MEDUSA, a stepwise approach based upon the Akaike information criterion for detecting multiple shifts in birth and death rates on an incompletely resolved phylogeny. We apply MEDUSA incompletely to a diversity tree summarizing both evolutionary relationships and species richness of 44 major clades of jawed vertebrates. We identify 9 major changes in the tempo of gnathostome diversification; the most significant of these lies at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. Rate increases also underlie several well recognized tetrapod radiations, including most modern birds, lizards and snakes, ostariophysan fishes, and most eutherian mammals. In addition, we find that large sections of the vertebrate tree exhibit nearly equal rates of origination and extinction, providing some of the first evidence from molecular data for the importance of faunal turnover in shaping biodiversity. Together, these results reveal living vertebrate biodiversity to be the product of volatile turnover punctuated by 6 accelerations responsible for >85% of all species as well as 3 slowdowns that have produced "living fossils." In addition, by revealing the timing of the exceptional pulses of vertebrate diversification as well as the clades that experience them, our diversity tree provides a framework for evaluating particular causal hypotheses of vertebrate radiations.
Rates of species origination and extinction can vary over time during evolutionary radiations, and it is possible to reconstruct the history of diversification using molecular phylogenies of extant taxa only. Maximum likelihood methods provide a useful framework for inferring temporal variation in diversification rates. LASER is a package for the R programming environment that implements maximum likelihood methods based on the birth-death process to test whether diversification rates have changed over time. LASER contrasts the likelihood of phylogenetic data under models where diversification rates have changed over time to alternative models where rates have remained constant over time. Major strengths of the package include the ability to detect temporal increases in diversification rates and the inference of diversification parameters under multiple rate-variable models of diversification. The program and associated documentation are freely available from the R package archive at http://cran.r-project.org.
The analysis of the tempo and mode of evolution has a strong tradition in paleontology. Recent advances in molecular phylogenetic reconstruction make it possible to complement this work by using data from extant species.
Phylogenies reconstructed from contemporary taxa do not contain information about lineages that have gone extinct. We derive probability models for such phylogenies, allowing real data to be compared with specified null models of evolution, and lineage birth and death rates to be estimated.
Felsenstein's maximum-likelihood approach for inferring phylogeny from DNA sequences assumes that the rate of nucleotide substitution is constant over different nucleotide sites. This assumption is sometimes unrealistic, as has been revealed by analysis of real sequence data. In the present paper Felsenstein's method is extended to the case where substitution rates over sites are described by the gamma distribution. A numerical example is presented to show that the method fits the data better than do previous models.
A simple model for the evolution of the rate of molecular evolution is presented. With a Bayesian approach, this model can serve as the basis for estimating dates of important evolutionary events even in the absence of the assumption of constant rates among evolutionary lineages. The method can be used in conjunction with any of the widely used models for nucleotide substitution or amino acid replacement. It is illustrated by analyzing a data set of rbcL protein sequences.
Analysis of Phylogenetics and Evolution (APE) is a package written in the R language for use in molecular evolution and phylogenetics.
APE provides both utility functions for reading and writing data and manipulating phylogenetic trees, as well as several advanced
methods for phylogenetic and evolutionary analysis (e.g. comparative and population genetic methods). APE takes advantage
of the many R functions for statistics and graphics, and also provides a flexible framework for developing and implementing
further statistical methods for the analysis of evolutionary processes.
Availability: The program is free and available from the official R package archive at http://cran.r-project.org/src/contrib/PACKAGES.html#ape. APE is licensed under the GNU General Public License.
The order Passeriformes ("perching birds") comprises extant species diversity comparable to that of living mammals. For over a decade, a single phylogenetic hypothesis based on DNA-DNA hybridization has provided the primary framework for numerous comparative analyses of passerine ecological and behavioral evolution and for tests of the causal factors accounting for rapid radiations within the group. We report here a strongly supported phylogenetic tree based on two single-copy nuclear gene sequences for the most complete sampling of passerine families to date. This tree is incongruent with that derived from DNA-DNA hybridization, with half of the nodes from the latter in conflict and over a third of the conflicts significant as assessed under maximum likelihood. Our historical framework suggests multiple waves of passerine dispersal from Australasia into Eurasia, Africa, and the New World, commencing as early as the Eocene, essentially reversing the classical scenario of oscine biogeography. The revised history implied by these data will require reassessment of comparative analyses of passerine diversification and adaptation.
Lineages that underwent rapid cladogenesis are attractive systems for the study of mechanisms underlying taxonomic, ecological, morphological, and behavioral diversification. Recently developed statistical methods provide insights into historical patterns of diversity and allow distinguishing bursts of cladogenesis from stochastic background rates in the presence of confounding factors such as extinction and incomplete taxon sampling. Here, we compare the dynamics of speciation in several marine fish lineages some of which were previously proposed to have undergone significant changes of cladogenesis through time. We tested for evidence of episodes of rapid cladogenesis using the constant rate and Monte Carlo constant rate tests that are robust to incomplete taxon sampling. These tests employ the statistic gamma to measure the relative position of internal node in a chronogram. For the first time, we conducted a comparative analysis to address the behavior of the statistic under different chronogram-constructing methods (Langley-Fitch, nonparametric rate smoothing, and penalized likelihood). Although estimates of gamma sometimes differ widely among methods, acceptance or rejection of the constant rate model within a particular clade appears to be robust to the choice of method. Bursts of cladogenesis were detected in 14 of 34 studied datasets. Some of these were previously proposed to represent marine fish "radiations," whereas others are identified anew. Our results indicate that the wider application of tree shape methods that are able to detect significantly elevated rates of speciation is useful to more precisely define clades that underwent episodes of rapid cladogenesis in marine fish clades. Contrasting the patterns of phylogenetic diversification in marine fish lineages may facilitate the identification of common evolutionary trajectories versus idiosyncrasies, and ultimately help towards a better understanding of the factors and processes underlying speciation in the marine realm.
In phylogenetics, the unrooted model of phylogeny and the strict molecular clock model are two extremes of a continuum. Despite their dominance in phylogenetic inference, it is evident that both are biologically unrealistic and that the real evolutionary process lies between these two extremes. Fortunately, intermediate models employing relaxed molecular clocks have been described. These models open the gate to a new field of "relaxed phylogenetics." Here we introduce a new approach to performing relaxed phylogenetic analysis. We describe how it can be used to estimate phylogenies and divergence times in the face of uncertainty in evolutionary rates and calibration times. Our approach also provides a means for measuring the clocklikeness of datasets and comparing this measure between different genes and phylogenies. We find no significant rate autocorrelation among branches in three large datasets, suggesting that autocorrelated models are not necessarily suitable for these data. In addition, we place these datasets on the continuum of clocklikeness between a strict molecular clock and the alternative unrooted extreme. Finally, we present analyses of 102 bacterial, 106 yeast, 61 plant, 99 metazoan, and 500 primate alignments. From these we conclude that our method is phylogenetically more accurate and precise than the traditional unrooted model while adding the ability to infer a timescale to evolution.
Determining whether speciation and extinction rates depend on the state of a particular character has been of long-standing interest to evolutionary biologists. To assess the effect of a character on diversification rates using likelihood methods requires that we be able to calculate the probability that a group of extant species would have evolved as observed, given a particular model of the character's effect. Here we describe how to calculate this probability for a phylogenetic tree and a two-state (binary) character under a simple model of evolution (the "BiSSE" model, binary-state speciation and extinction). The model involves six parameters, specifying two speciation rates (rate when the lineage is in state 0; rate when in state 1), two extinction rates (when in state 0; when in state 1), and two rates of character state change (from 0 to 1, and from 1 to 0). Using these probability calculations, we can do maximum likelihood inference to estimate the model's parameters and perform hypothesis tests (e.g., is the rate of speciation elevated for one character state over the other?). We demonstrate the application of the method using simulated data with known parameter values.
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.
The disparity in species richness among groups of organisms is one of the most pervasive features of life on earth. A number of studies have addressed this pattern across higher taxa (e.g. 'beetles'), but we know much less about the generality and causal basis of the variation in diversity within evolutionary radiations at lower taxonomic scales. Here, we address the causes of variation in species richness among major lineages of Australia's most diverse vertebrate radiation, a clade of at least 232 species of scincid lizards. We use new mitochondrial and nuclear intron DNA sequences to test the extent of diversification rate variation in this group. We present an improved likelihood-based method for estimating per-lineage diversification rates from combined phylogenetic and taxonomic (species richness) data, and use the method in a hypothesis-testing framework to localize diversification rate shifts on phylogenetic trees. We soundly reject homogeneity of diversification rates among members of this radiation, and find evidence for a dramatic rate increase in the common ancestor of the genera Ctenotus and Lerista. Our results suggest that the evolution of traits associated with climate tolerance may have had a role in shaping patterns of diversity in this group.
Aspects of phylogenetic tree shape, and in particular tree balance, provide clues to the workings of the macroevolutionary process. I use a simulation approach to explore patterns in tree balance for several models of the evolutionary process under which speciation rates vary through the history of diversifying clades. I demonstrate that when speciation rates depend on an evolving trait of individuals, and are therefore "heritable" along evolutionary lineages, the resulting phylogenies become imbalanced. However, imbalance also results from some (but not all) models of "nonheritable" speciation rate variation. The degree of imbalance increases with the magnitude of speciation rate variation, and then for gradual evolution (but not punctuated equilibria) reaches an asymptote short of the theoretical maximum. Very high levels of rate variation are required to produce imbalance matching that found in real data (estimated phylogenies from the systematic literature). I discuss implications of the simulation results for our understanding of macroevolution.
Phylogenies reconstructed from gene sequences can be used to investigate the tempo and mode of species diversification. Here we develop and use new statistical methods to infer past patterns of speciation and extinction from molecular phylogenies. Specifically, we test the null hypothesis that per-lineage speciation and extinction rates have remained constant through time. Rejection of this hypothesis may provide evidence for evolutionary events such as adaptive radiations or key adaptations. In contrast to previous approaches, our methods are robust to incomplete taxon sampling and are conservative with respect to extinction. Using simulation we investigate, first, the adverse effects of failing to take incomplete sampling into account and, second, the power and reliability of our tests. When applied to published phylogenies our tests suggest that, in some cases, speciation rates have decreased through time.
What are supertrees and what is all the fuss about?
The well-known decline of global background extinction intensity was caused by the sorting of higher taxonomic groups. Two factors were responsible. First, probabilities of familial origination and extinction in these groups (taxonomic orders) were highly correlated. Groups whose families had high probabilities of origination and extinction tended to have highly volatile diversity paths and, consequently, short life spans. Second, orders with high probabilities of familial origination and extinction were rarely replaced by new high-turnover orders. Thus, because high-turnover orders tended to become extinct without replacement, the global background extinction intensity declined. Since familial origination and extinction probabilities are correlated, global background origination intensity inevitably declined as well. As a consequence of these processes, virtually all groups of organisms now living have low probabilities of familial origination and extinction.
Simulations of branching evolution were used to obtain the expected relationships among probabilities (of origination and extinction), volatilities, and longevities for the entire range of possible probabilities, and these relationships were compared to those obtained from the empirical record. In the simulations, only the probabilities of origination and extinction were specified, so volatilities and clade longevities were determined entirely by the probabilities. The similarity between results obtained by simulation and those obtained by analysis of the empirical record further supports the inference that the observed decline of background extinction (and origination) intensity can be explained largely by the loss of high-probability groups to induced volatility.
The evolutionary pattern of speciation and extinction in any biologic group may be described by a variety of mathematical models. These models provide a framework for describing the history of taxonomic diversity (clade shape) and other aspects of large evolutionary patterns. The simplest model assumes time homogeneity; that is, speciation and extinction probabilities are constant through time and within taxonomic groups. In some cases, the homogeneous model provides a good fit to real world paleontological data, but in other cases the model serves only as a null hypothesis that must be rejected before more complex models can be applied. In cases where the homogeneous model does not fit the data, time-inhomogeneous models can be formulated that specify change, regular or episodic, in speciation and extinction probabilities. An appendix provides a list of the most useful equations based on the homogeneous model.-Author
Aspects of phylogenetic tree shape, and in particular tree balance, provide clues to the workings of the macroevolutionary process. I use a simulation approach to explore patterns in tree balance for several models of the evolutionary process under which speciation rates vary through the history of diversifying clades. I demonstrate that when speciation rates depend on an evolving trait of individuals, and are therefore 'heritable' along evolutionary lineages, the resulting phylogenies become imbalanced. However, imbalance also results from some (but not all) models of 'nonheritable' speciation rate variation. The degree of imbalance increases with the magnitude of speciation rate variation, and then for gradual evolution (but not punctuated equilibria) reaches an asymptote short of the theoretical maximum. Very high levels of rate variation are required to produce imbalance matching that found in real data (estimated phylogenies from the systematic literature). I discuss implications of the simulation results for our understanding of macroevolution.
Birth-death models, and their subsets—the pure birth and pure death models—have a long history of use for informing thinking about macroevolutionary patterns. Here we illustrate with examples the wide range of questions they have been used to address, including estimating and comparing rates of diversification of clades, investi-gating the "shapes" of clades, and some rather surprising uses such as estimating speciation rates from data that are not resolved below the level of the genus. The raw data for inference can be the fossil record or the molecular phylogeny of a clade, and we explore the similarites and differences in the behavior of the birth-death models when applied to these different forms of data.
This paper documents a series of methodological innovations that are relevant to mac-roevolutionary studies. The new methods are applied to updated faunal and body mass data sets for North American fossil mammals, documenting several key trends across the late Cretaceous and Cenozoic. The methods are (1) A maximum likelihood formulation of appearance event or-dination. The reformulated criterion involves generating a maximally likely hypothesized relative ordering of first and last appearances (i.e., an age range chart). The criterion takes faunal occur-rences, stratigraphic relationships, and the sampling probability of individual genera and species into account. (2) A nonparametric temporal interpolation method called ''shrink-wrapping'' that makes it possible to employ the greatest possible number of tie points without violating monoto-nicity or allowing abrupt changes in slopes. The new calibration method is used in computing pro-visional definitions of boundaries among North American land mammal ages. (3) Additional meth-ods for randomized subsampling of faunal lists, one weighting the number of lists that have been drawn by the sum of the square of the number of occurrences in each list, and one further modi-fying this approach to account for long-term changes in average local species richness. (4) Foote's new equations for instantaneous speciation and extinction rates. The equations are rederived and used to generate time series, confirm that logistic dynamics result from the diversity dependence of speciation but not extinction, and define the median duration of species (i.e., 2.6 m.y. for Eocene– Pleistocene mammals). (5) A method employing the G likelihood ratio statistic that is used to quan-tify the volatility of changes in the relative proportion of species falling in each of several major taxonomic groups. (6) Univariate measures of body mass distributions based on ordinary moment statistics (mean, standard deviation, skewness, kurtosis). These measures are favored over the method of cenogram analysis. Data are presented showing that even diverse individual fossil col-lections merely yield a noisy version of the same pattern seen in the overall continental data set. Peaks in speciation rates, extinction rates, proportional volatility, and shifts in body mass distri-butions occur at different times, suggesting that environmental perturbations do not have simple effects on the biota.
Abstract The extraordinary contemporary species richness and ecological predominance of flowering plants (angiosperms) are even more remarkable when considering the relatively recent onset of their evolutionary diversification. We examine the evolutionary diversification of angiosperms and the observed differential distribution of species in angiosperm clades by estimating the rate of diversification for angiosperms as a whole and for a large set of angiosperm clades. We also identify angiosperm clades with a standing diversity that is either much higher or lower than expected, given the estimated background diversification rate. Recognition of angiosperm clades, the phylogenetic relationships among them, and their taxonomic composition are based on an empirical compilation of primary phylogenetic studies. By making an integrative and critical use of the paleobotanical record, we obtain reasonably secure approximations for the age of a large set of angiosperm clades. Diversification was modeled as a stochastic, time-homogeneous birth-and-death process that depends on the diversification rate (r) and the relative extinction rate (∈). A statistical analysis of the birth and death process was then used to obtain 95% confidence intervals for the expected number of species through time in a clade that diversifies at a rate equal to that of angiosperms as a whole. Confidence intervals were obtained for stem group and for crown group ages in the absence of extinction (∈= 0.0) and under a high relative extinction rate (∈= 0.9). The standing diversity of angiosperm clades was then compared to expected species diversity according to the background rate of diversification, and, depending on their placement with respect to the calculated confidence intervals, exceedingly species-rich or exceedingly species-poor clades were identified. The rate of diversification for angiosperms as a whole ranges from 0.077 (∈= 0.9) to 0.089 (∈= 0.0) net speciation events per million years. Ten clades fall above the confidence intervals of expected species diversity, and 13 clades were found to be unexpectedly species poor. The phylogenetic distribution of clades with an exceedingly high number of species suggests that traits that confer high rates of diversification evolved independently in different instances and do not characterize the angiosperms as a whole.
The extraordinary diversity of angiosperms is the ultimate outcome of the interplay of speciation and extinction, which determine the net diversification of different lineages. We document the temporal trends of angiosperm diversification rates during their early history. Absolute diversification rates were estimated for order-level clades using ages derived from relaxed molecular clock analyses that included or excluded a maximal constraint to angiosperm age. Diversification rates for angiosperms as a whole ranged from 0.0781 to 0.0909 net speciation events per million years, with dates from the constrained analysis. Diversification through time plots show an inverse relationship between clade age and rate, where the younger clades tend to have the highest rates. Angiosperm diversity is found to have mixed origins: slightly less than half of the living species belong to lineages with low to moderate diversification rates, which appeared between 130 and 102 Mya (Barremian-uppermost Albian; Lower Cretaceous). Slightly over half of the living species belong to lineages with moderate to high diversification rates, which appeared between 102 and 77 Mya (Cenomanian-mid Campanian; Upper Cretaceous). Terminal lineages leading to living angiosperm species, however, may have originated soon or long after the phylogenetic differentiation of the clade to which they belong.
Time-calibrated molecular phylogenies provide a valuable window into the tempo and mode of species diversification, especially for the large number of groups that lack adequate fossil records. Molecular phylogenetic data frequently suggest an initial "explosive speciation" phase, leading to widespread speculation that ecological niche-filling processes might govern the dynamics of species diversification during evolutionary radiations. However, these patterns are difficult to reconcile with the fossil record. The fossil record strongly suggests that extinction rates have been high relative to speciation rates, but such elevated background extinction should erase the signal of early, rapid speciation from molecular phylogenies. For this reason, extinction rates in molecular phylogenies are frequently estimated as zero under the widely used birth-death model. Here, I construct a simple model that combines phylogenetically patterned extinction with pulsed turnover dynamics and constant diversity through time. Using approximate Bayesian methods, I show that heritable extinction can easily explain the phenomenon of explosive early diversification, even when net diversification rates are equal to zero. Several assumptions of the model are more consistent with both the fossil record and neontological data than the standard birth-death model and it may thus represent a viable alternative interpretation of phylogenetic diversification patterns. These results suggest that variation in the absolute rate of lineage turnover through time, in conjunction with phylogenetically nonrandom extinction, may underlie the apparent diversity-dependent speciation observed in molecular phylogenies.
Recent application of time-varying birth-death models to molecular phylogenies suggests that a decreasing diversification rate can only be observed if there was a decreasing speciation rate coupled with extremely low or no extinction. However, from a paleontological perspective, zero extinction rates during evolutionary radiations seem unlikely. Here, with a more comprehensive set of computer simulations, we show that substantial extinction can occur without erasing the signal of decreasing diversification rate in a molecular phylogeny. We also find, in agreement with the previous work, that a decrease in diversification rate cannot be observed in a molecular phylogeny with an increasing extinction rate alone. Further, we find that the ability to observe decreasing diversification rates in molecular phylogenies is controlled (in part) by the ratio of the initial speciation rate (Lambda) to the extinction rate (Mu) at equilibrium (the LiMe ratio), and not by their absolute values. Here we show in principle, how estimates of initial speciation rates may be calculated using both the fossil record and the shape of lineage through time plots derived from molecular phylogenies. This is important because the fossil record provides more reliable estimates of equilibrium extinction rates than initial speciation rates.
How biodiversity is generated and maintained underlies many major questions in evolutionary biology, particularly relating to the tempo and pattern of diversification through time. Molecular phylogenies and new analytical methods provide additional tools to help interpret evolutionary processes. Evolutionary rates in lineages sometimes appear punctuated, and such "explosive" radiations are commonly interpreted as adaptive, leading to causative key innovations being sought. Here we argue that an alternative process might explain apparently rapid radiations ("broom-and-handle" or "stemmy" patterns seen in many phylogenies) with no need to invoke dramatic increase in the rate of diversification. We use simulations to show that mass extinction events can produce the same phylogenetic pattern as that currently being interpreted as due to an adaptive radiation. By comparing simulated and empirical phylogenies of Australian and southern African legumes, we find evidence for coincident mass extinctions in multiple lineages that could have resulted from global climate change at the end of the Eocene.
Species richness varies dramatically among groups of organisms, yet the causes of this variation remain poorly understood. Variation in species-level diversification rates may partially explain differential species richness among clades, but older clades should also be more diverse, because they will have had more time to accumulate species. Surprisingly, studies that have investigated this question have reached dramatically different conclusions: several claim to find no such age-diversity relationship, whereas a recent and more inclusive study reported that clade age and not diversification rate explains the variation in species richness among animal taxa. Here I address the relationship between clade age and species richness using a model-based approach that controls for variation in diversification rates among clades. I find that species richness is effectively independent of clade age in four of five data sets. Even extreme among-clade variation in diversification rates cannot account for the absence of a positive age-diversity relationship in angiosperms, birds, and teleost fishes. I consider two alternative explanations for these results and find that a clade volatility model positing correlated speciation-extinction dynamics does not underlie these patterns. Rather, ecological limits on clade growth, such as geographic area, appear to mediate temporal declines in diversification within higher taxa.
Clades diversify in an ecological context, but most macroevolutionary models do not directly encapsulate ecological mechanisms that influence speciation and extinction. A data set of 245 chordate, arthropod, mollusk, and magnoliophyte phylogenies had a majority of clades that showed rapid lineage accumulation early with a slowing more recently, whereas a small but significant minority showed accelerated lineage accumulation in their recent histories. Previous analyses have demonstrated that macroevolutionary birth-death models can replicate the pattern of slowing lineage accumulation only by a strong decrease in speciation rate with increasing species richness and extinction rate held extremely low or absent. In contrast, the metacommunity model presented here could generate the full range of patterns seen in the real phylogenies by simply manipulating the degree of ecological differentiation of new species at the time of speciation. Specifically, the metacommunity model predicts that clades showing decelerating lineage accumulation rates are those that have diversified by ecological modes of speciation, whereas clades showing accelerating lineage accumulation rates are those that have diversified primarily by modes of speciation that generate little or no ecological diversification. A number of testable predictions that integrate data from molecular systematics, community ecology, and biogeography are also discussed.
The discipline-wide effort to database the fossil record at the occurrence level has made it possible to estimate marine invertebrate extinction and origination rates with much greater accuracy. The new data show that two biotic mechanisms have hastened recoveries from mass extinctions and confined diversity to a relatively narrow range over the past 500 million years (Myr). First, a drop in diversity of any size correlates with low extinction rates immediately afterward, so much so that extinction would almost come to a halt if diversity dropped by 90%. Second, very high extinction rates are followed by equally high origination rates. The two relationships predict that the rebound from the current mass extinction will take at least 10 Myr, and perhaps 40 Myr if it rivals the Permo-Triassic catastrophe. Regardless, any large event will result in a dramatic ecological and taxonomic restructuring of the biosphere. The data also confirm that extinction and origination rates both declined through the Phanerozoic and that several extinctions in addition to the Permo-Triassic event were particularly severe. However, the trend may be driven by taxonomic biases and the rates vary in accord with a simple log normal distribution, so there is no sharp distinction between background and mass extinctions. Furthermore, the lack of any significant autocorrelation in the data is inconsistent with macroevolutionary theories of periodicity or self-organized criticality.
Molecular phylogenies can be used to reject null models of the way we think evolution occurred, including patterns of lineage extinction. They can also be used to provide maximum likelihood estimates of parameters associated with lineage birth and death rates. We illustrate: (i) how molecular phylogenies provide information about the extent to which particular clades are likely to be under threat from extinction; (ii) how cursory analyses of molecular phylogenies can lead to incorrect conclusions about the evolutionary processes that have been at work; and (iii) how different evolutionary processes leave distinctive marks on the structure of reconstructed phylogenies.
Phylogenies reconstructed from gene sequences can be used to investigate the tempo and mode of species diversification. Here we develop and use new statistical methods to infer past patterns of speciation and extinction from molecular phylogenies. Specifically, we test the null hypothesis that per-lineage speciation and extinction rates have remained constant through time. Rejection of this hypothesis may provide evidence for evolutionary events such as adaptive radiations or key adaptations. In contrast to previous approaches, our methods are robust to incomplete taxon sampling and are conservative with respect to extinction. Using simulation we investigate, first, the adverse effects of failing to take incomplete sampling into account and, second, the power and reliability of our tests. When applied to published phylogenies our tests suggest that, in some cases, speciation rates have decreased through time.
The extraordinary contemporary species richness and ecological predominance of flowering plants (angiosperms) are even more remarkable when considering the relatively recent onset of their evolutionary diversification. We examine the evolutionary diversification of angiosperms and the observed differential distribution of species in angiosperm clades by estimating the rate of diversification for angiosperms as a whole and for a large set of angiosperm clades. We also identify angiosperm clades with a standing diversity that is either much higher or lower than expected, given the estimated background diversification rate. Recognition of angiosperm clades, the phylogenetic relationships among them, and their taxonomic composition are based on an empirical compilation of primary phylogenetic studies. By making an integrative and critical use of the paleobotanical record, we obtain reasonably secure approximations for the age of a large set of angiosperm clades. Diversification was modeled as a stochastic, time-homogeneous birth-and-death process that depends on the diversification rate (r) and the relative extinction rate (epsilon). A statistical analysis of the birth and death process was then used to obtain 95% confidence intervals for the expected number of species through time in a clade that diversifies at a rate equal to that of angiosperms as a whole. Confidence intervals were obtained for stem group and for crown group ages in the absence of extinction (e = 0.0) and under a high relative extinction rate (epsilon = 0.9). The standing diversity of angiosperm clades was then compared to expected species diversity according to the background rate of diversification, and, depending on their placement with respect to the calculated confidence intervals, exceedingly species-rich or exceedingly species-poor clades were identified. The rate of diversification for angiosperms as a whole ranges from 0.077 (epsilon = 0.9) to 0.089 (epsilon = 0.0) net speciation events per million years. Ten clades fall above the confidence intervals of expected species diversity, and 13 clades were found to be unexpectedly species poor. The phylogenetic distribution of clades with an exceedingly high number of species suggests that traits that confer high rates of diversification evolved independently in different instances and do not characterize the angiosperms as a whole.
Identification of general properties of evolutionary radiations has been hindered by the lack of a general statistical and phylogenetic approach applicable across diverse taxa. We present a comparative analytical framework for examining phylogenetic patterns of diversification and morphological disparity with data from four iguanian-lizard taxa that exhibit substantially different patterns of evolution. Taxa whose diversification occurred disproportionately early in their evolutionary history partition more of their morphological disparity among, rather than within, subclades. This inverse relationship between timing of diversification and morphological disparity within subclades may be a general feature that transcends the historically contingent properties of different evolutionary radiations.
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 estimation of diversification rates using phylogenetic data has attracted a lot of attention in the past decade. In this context, the analysis of incomplete phylogenies (e.g. phylogenies resolved at the family level but unresolved at the species level) has remained difficult. I present here a likelihood-based method to combine partly resolved phylogenies with taxonomic (species-richness) data to estimate speciation and extinction rates. This method is based on fitting a birth-and-death model to both phylogenetic and taxonomic data. Some examples of the method are presented with data on birds and on mammals. The method is compared with existing approaches that deal with incomplete phylogenies. Some applications and generalizations of the approach introduced in this paper are further discussed.
Taxa differ widely in numbers of species, which may be due either to chance alone or to factors that cause differences in speciation and extinction rates between taxa. To test whether an observed distribution of species over taxa differs from the distribution expected from chance alone, one must take into account that neither speciation nor extinction rates are known. This paper introduces a way to estimate speciation and extinction probabilities from the distribution of extant species over families and to test whether the observed distribution is different from expected. Application of this procedure to the distributions of bird, hexapod, primate, and angiosperm species over taxa provides statistical evidence of differences in rates of cladogenesis between taxa.
There is considerable interest in the possibility of using molecular phylogenies to estimate extinction rates. The present study aims at assessing the statistical performance of the birth-death model fitting approach to estimate speciation and extinction rates by comparison to the approach considering fossil data. A simulation-based approach was used. The diversification of a large number of lineages was simulated under a wide range of speciation and extinction rate values. The estimators obtained with fossils performed better than those without fossils. In the absence of fossils (e.g. with a molecular phylogeny), the speciation rate was correctly estimated in a wide range of situations; the bias of the corresponding estimator was close to zero for the largest trees. However, this estimator was substantially biased when the simulated extinction rate was high. On the other hand the estimator of extinction rate was biased in a wide range of situations. Surprisingly, this bias was lesser with medium-sized trees. Some recommendations for interpreting results from a diversification analysis are given.
Maximum likelihood is a potentially powerful approach for investigating the tempo of diversification using molecular phylogenetic data. Likelihood methods distinguish between rate-constant and rate-variable models of diversification by fitting birth-death models to phylogenetic data. Because model selection in this context is a test of the null hypothesis that diversification rates have been constant over time, strategies for selecting best-fit models must minimize Type I error rates while retaining power to detect rate variation when it is present. Here I examine model selection, parameter estimation, and power to reject the null hypothesis using likelihood models based on the birth-death process. The Akaike information criterion (AIC) has often been used to select among diversification models; however, I find that selecting models based on the lowest AIC score leads to a dramatic inflation of the Type I error rate. When appropriately corrected to reduce Type I error rates, the birth-death likelihood approach performs as well or better than the widely used gamma statistic, at least when diversification rates have shifted abruptly over time. Analyses of datasets simulated under a range of rate-variable diversification scenarios indicate that the birth-death likelihood method has much greater power to detect variation in diversification rates when extinction is present. Furthermore, this method appears to be the only approach available that can distinguish between a temporal increase in diversification rates and a rate-constant model with nonzero extinction. I illustrate use of the method by analyzing a published phylogeny for Australian agamid lizards.
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.
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.
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.
