A global reptile assessment highlights shared conservation needs of tetrapods.

Comprehensive assessments of species' extinction risks have documented the extinction crisis1 and underpinned strategies for reducing those risks2. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and 13.6% of birds are threatened with extinction3. Because global assessments have been lacking, reptiles have been omitted from conservation-prioritization analyses that encompass other tetrapods4-7. Reptiles are unusually diverse in arid regions, suggesting that they may have different conservation needs6. Here we provide a comprehensive extinction-risk assessment of reptiles and show that at least 1,829 out of 10,196 species (21.1%) are threatened-confirming a previous extrapolation8 and representing 15.6 billion years of phylogenetic diversity. Reptiles are threatened by the same major factors that threaten other tetrapods-agriculture, logging, urban development and invasive species-although the threat posed by climate change remains uncertain. Reptiles inhabiting forests, where these threats are strongest, are more threatened than those in arid habitats, contrary to our prediction. Birds, mammals and amphibians are unexpectedly good surrogates for the conservation of reptiles, although threatened reptiles with the smallest ranges tend to be isolated from other threatened tetrapods. Although some reptiles-including most species of crocodiles and turtles-require urgent, targeted action to prevent extinctions, efforts to protect other tetrapods, such as habitat preservation and control of trade and invasive species, will probably also benefit many reptiles.

Discovering research articles containing evolutionary timetrees by machine learning.

MOTIVATION: Timetrees depict evolutionary relationships between species and the geological times of their divergence. Hundreds of research articles containing timetrees are published in scientific journals every year. The TimeTree (TT) project has been manually locating, curating and synthesizing timetrees from these articles for almost two decades into a TimeTree of Life, delivered through a unique, user-friendly web interface (timetree.org). The manual process of finding articles containing timetrees is becoming increasingly expensive and time-consuming. So, we have explored the effectiveness of text-mining approaches and developed optimizations to find research articles containing timetrees automatically. RESULTS: We have developed an optimized machine learning system to determine if a research article contains an evolutionary timetree appropriate for inclusion in the TT resource. We found that BERT classification fine-tuned on whole-text articles achieved an F1 score of 0.67, which we increased to 0.88 by text-mining article excerpts surrounding the mentioning of figures. The new method is implemented in the TimeTreeFinder (TTF) tool, which automatically processes millions of articles to discover timetree-containing articles. We estimate that the TTF tool would produce twice as many timetree-containing articles as those discovered manually, whose inclusion in the TT database would potentially double the knowledge accessible to a wider community. Manual inspection showed that the precision on out-of-distribution recently published articles is 87%. This automation will speed up the collection and curation of timetrees with much lower human and time costs. AVAILABILITY AND IMPLEMENTATION: https://github.com/marija-stanojevic/time-tree-classification. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Limitations of Phylogenomic Data Can Drive Inferred Speciation Rate Shifts.

Biodiversity analyses of phylogenomic timetrees have produced many high-profile examples of shifts in the rate of speciation across the tree of life. Temporally correlated events in ecology, climate, and biogeography are frequently invoked to explain these rate shifts. In a re-examination of 15 genomic timetrees and 25 major published studies of the pattern of speciation through time, we observed an unexpected correlation between the timing of reported rate shifts and the information content of sequence alignments. Here, we show that the paucity of sequence variation and insufficient species sampling in phylogenomic data sets are the likely drivers of many inferred speciation rate shifts, rather than the proposed biological explanations. Therefore, data limitations can produce predictable but spurious signals of rate shifts even when speciation rates may be similar across taxa and time. Our results suggest that the reliable detection of speciation rate shifts requires the acquisition and assembly of long phylogenomic alignments with near-complete species sampling and accurate estimates of species richness for the clades of study.

TimeTree 5: An Expanded Resource for Species Divergence Times.

We present the fifth edition of the TimeTree of Life resource (TToL5), a product of the timetree of life project that aims to synthesize published molecular timetrees and make evolutionary knowledge easily accessible to all. Using the TToL5 web portal, users can retrieve published studies and divergence times between species, the timeline of a species' evolution beginning with the origin of life, and the timetree for a given evolutionary group at the desired taxonomic rank. TToL5 contains divergence time information on 137,306 species, 41% more than the previous edition. The TToL5 web interface is now ADA-compliant and mobile-friendly, a result of comprehensive source code refactoring. TToL5 also offers programmatic access to species divergence times and timelines through an application programming interface, which is accessible at timetree.temple.edu/api. TToL5 is publicly available at timetree.org.

Large-Scale Phylogenomic Analyses Reveal the Monophyly of Bryophytes and Neoproterozoic Origin of Land Plants.

The relationships among the four major embryophyte lineages (mosses, liverworts, hornworts, vascular plants) and the timing of the origin of land plants are enigmatic problems in plant evolution. Here, we resolve the monophyly of bryophytes by improving taxon sampling of hornworts and eliminating the effect of synonymous substitutions. We then estimate the divergence time of crown embryophytes based on three fossil calibration strategies, and reveal that maximum calibration constraints have a major effect on estimating the time of origin of land plants. Moreover, comparison of priors and posteriors provides a guide for evaluating the optimal calibration strategy. By considering the reliability of fossil calibrations and the influences of molecular data, we estimate that land plants originated in the Precambrian (980-682 Ma), much older than widely recognized. Our study highlights the important contribution of molecular data when faced with contentious fossil evidence, and that fossil calibrations used in estimating the timescale of plant evolution require critical scrutiny.

Haiti's biodiversity threatened by nearly complete loss of primary forest.

Tropical forests hold most of Earth's biodiversity. Their continued loss through deforestation and agriculture is the main threat to species globally, more than disease, invasive species, and climate change. However, not all tropical forests have the same ability to sustain biodiversity. Those that have been disturbed by humans, including forests previously cleared and regrown (secondary growth), have lower levels of species richness compared with undisturbed (primary) forests. The difference is even greater considering extinctions that will later emanate from the disturbance (extinction debt). Here, we find that Haiti has less than 1% of its original primary forest and is therefore among the most deforested countries. Primary forest has declined over three decades inside national parks, and 42 of the 50 highest and largest mountains have lost all primary forest. Our surveys of vertebrate diversity (especially amphibians and reptiles) on mountaintops indicates that endemic species have been lost along with the loss of forest. At the current rate, Haiti will lose essentially all of its primary forest during the next two decades and is already undergoing a mass extinction of its biodiversity because of deforestation. These findings point to the need, in general, for better reporting of forest cover data of relevance to biodiversity, instead of "total forest" as defined by the United Nation's Food and Agricultural Organization. Expanded detection and monitoring of primary forest globally will improve the efficiency of conservation measures, inside and outside of protected areas.

Global priorities for conservation across multiple dimensions of mammalian diversity.

Conservation priorities that are based on species distribution, endemism, and vulnerability may underrepresent biologically unique species as well as their functional roles and evolutionary histories. To ensure that priorities are biologically comprehensive, multiple dimensions of diversity must be considered. Further, understanding how the different dimensions relate to one another spatially is important for conservation prioritization, but the relationship remains poorly understood. Here, we use spatial conservation planning to (i) identify and compare priority regions for global mammal conservation across three key dimensions of biodiversity-taxonomic, phylogenetic, and traits-and (ii) determine the overlap of these regions with the locations of threatened species and existing protected areas. We show that priority areas for mammal conservation exhibit low overlap across the three dimensions, highlighting the need for an integrative approach for biodiversity conservation. Additionally, currently protected areas poorly represent the three dimensions of mammalian biodiversity. We identify areas of high conservation priority among and across the dimensions that should receive special attention for expanding the global protected area network. These high-priority areas, combined with areas of high priority for other taxonomic groups and with social, economic, and political considerations, provide a biological foundation for future conservation planning efforts.

Undersampling Genomes has Biased Time and Rate Estimates Throughout the Tree of Life.

Genomic data drive evolutionary research on the relationships and timescale of life but the genomes of most species remain poorly sampled. Phylogenetic trees can be reconstructed reliably using small data sets and the same has been assumed for the estimation of divergence time with molecular clocks. However, we show here that undersampling of molecular data results in a bias expressed as disproportionately shorter branch lengths and underestimated divergence times in the youngest nodes and branches, termed the small sample artifact. In turn, this leads to increasing speciation and diversification rates towards the present. Any evolutionary analyses derived from these biased branch lengths and speciation rates will be similarly biased. The widely used timetrees of the major species-rich studies of amphibians, birds, mammals, and squamate reptiles are all data-poor and show upswings in diversification rate, suggesting that their results were biased by undersampling. Our results show that greater sampling of genomes is needed for accurate time and rate estimation, which are basic data used in ecological and evolutionary research.

The Timetree of Prokaryotes: New Insights into Their Evolution and Speciation.

The increasing size of timetrees in recent years has led to a focus on diversification analyses to better understand patterns of macroevolution. Thus far, nearly all studies have been conducted with eukaryotes primarily because phylogenies have been more difficult to reconstruct and calibrate to geologic time in prokaryotes. Here, we have estimated a timetree of 11,784 'species' of prokaryotes and explored their pattern of diversification. We used data from the small subunit ribosomal RNA along with an evolutionary framework from previous multi-gene studies to produce three alternative timetrees. For each timetree we surprisingly found a constant net diversification rate derived from an exponential increase of lineages and showing no evidence of saturation (rate decline), the same pattern found previously in eukaryotes. The implication is that prokaryote diversification as a whole is the result of the random splitting of lineages and is neither limited by existing diversity (filled niches) nor responsive in any major way to environmental changes.

TimeTree: A Resource for Timelines, Timetrees, and Divergence Times.

Evolutionary information on species divergence times is fundamental to studies of biodiversity, development, and disease. Molecular dating has enhanced our understanding of the temporal patterns of species divergences over the last five decades, and the number of studies is increasing quickly due to an exponential growth in the available collection of molecular sequences from diverse species and large number of genes. Our TimeTree resource is a public knowledge-base with the primary focus to make available all species divergence times derived using molecular sequence data to scientists, educators, and the general public in a consistent and accessible format. Here, we report a major expansion of the TimeTree resource, which more than triples the number of species (>97,000) and more than triples the number of studies assembled (>3,000). Furthermore, scientists can access not only the divergence time between two species or higher taxa, but also a timetree of a group of species and a timeline that traces a species' evolution through time. The new timetree and timeline visualizations are integrated with display of events on earth and environmental history over geological time, which will lead to broader and better understanding of the interplay of the change in the biosphere with the diversity of species on Earth. The next generation TimeTree resource is publicly available online at http://www.timetree.org.

Evolutionary time drives global tetrapod diversity.

Global variation in species richness is widely recognized, but the explanation for what drives it continues to be debated. Previous efforts have focused on a subset of potential drivers, including evolutionary rate, evolutionary time (maximum clade age of species restricted to a region), dispersal (migration from one region to another), ecological factors and climatic stability. However, no study has evaluated these competing hypotheses simultaneously at a broad spatial scale. Here, we examine their relative contribution in determining the richness of the most comprehensive dataset of tetrapods to our knowledge (84% of the described species), distinguishing between the direct influences of evolutionary rate, evolutionary time and dispersal, and the indirect influences of ecological factors and climatic stability through their effect on direct factors. We found that evolutionary time exerted a primary influence on species richness, with evolutionary rate being of secondary importance. By contrast, dispersal did not significantly affect richness patterns. Ecological and climatic stability factors influenced species richness indirectly by modifying evolutionary time (i.e. persistence time) and rate. Overall, our findings suggest that global heterogeneity in tetrapod richness is explained primarily by the length of time species have had to diversify.

Phylogenomic support for evolutionary relationships of New World direct-developing frogs (Anura: Terraranae).

Phylogenomic approaches have proven able to resolve difficult branches in the tree of life. New World direct-developing frogs (Terraranae) represent a large evolutionary radiation in which interrelationships at key points in the phylogeny have not been adequately determined, affecting evolutionary, biogeographic, and taxonomic interpretations. We employed anchored hybrid enrichment to generate a data set containing 389 loci and >600,000 nucleotide positions for 30 terraranan and several outgroup frog species encompassing all major lineages in the clade. Concatenated maximum likelihood and coalescent species-tree approaches recover nearly identical topologies with strong support for nearly all relationships in the tree. These results are similar to previous phylogenetic results but provide additional resolution at short internodes. Among taxa whose placement varied in previous analyses, Ceuthomantis is shown to be the sister taxon to all other terraranans, rather than deeply embedded within the radiation, and Strabomantidae is monophyletic rather than paraphyletic with respect to Craugastoridae. We present an updated taxonomy to reflect these results, and describe a new subfamily for the genus Hypodactylus.

Molecular evidence for the paraphyly of Scolecophidia and its evolutionary implications.

The phylogenetic relationships between the three main clades of worm snakes remain controversial. This question is, however, crucial to elucidate the origin of the successful snake radiation, as these burrowing and miniaturized wormlike organisms represent the earliest branching clades within the snake tree. The present molecular phylogenetic study, intended to minimize the amount of missing data, provides fully resolved inter-subfamilial relationships among Typhlopidae. It also brings robust evidence that worm snakes (Scolecophidia) are paraphyletic, with the scolecophidian family Anomalepididae recovered with strong support as sister clade to the 'typical snakes' (Alethinophidia). Ancestral state reconstructions applied to three different traits strongly associated to a burrowing life-style (scolecoidy, absence of retinal cones and microstomy) provide results in favour of a burrowing origin of snakes, and suggest that worm snakes might be the only extant fossorial representatives of the primordial snake incursion towards an underground environment.

Advances in Time Estimation Methods for Molecular Data.

Molecular dating has become central to placing a temporal dimension on the tree of life. Methods for estimating divergence times have been developed for over 50 years, beginning with the proposal of molecular clock in 1962. We categorize the chronological development of these methods into four generations based on the timing of their origin. In the first generation approaches (1960s-1980s), a strict molecular clock was assumed to date divergences. In the second generation approaches (1990s), the equality of evolutionary rates between species was first tested and then a strict molecular clock applied to estimate divergence times. The third generation approaches (since ∼2000) account for differences in evolutionary rates across the tree by using a statistical model, obviating the need to assume a clock or to test the equality of evolutionary rates among species. Bayesian methods in the third generation require a specific or uniform prior on the speciation-process and enable the inclusion of uncertainty in clock calibrations. The fourth generation approaches (since 2012) allow rates to vary from branch to branch, but do not need prior selection of a statistical model to describe the rate variation or the specification of speciation model. With high accuracy, comparable to Bayesian approaches, and speeds that are orders of magnitude faster, fourth generation methods are able to produce reliable timetrees of thousands of species using genome scale data. We found that early time estimates from second generation studies are similar to those of third and fourth generation studies, indicating that methodological advances have not fundamentally altered the timetree of life, but rather have facilitated time estimation by enabling the inclusion of more species. Nonetheless, we feel an urgent need for testing the accuracy and precision of third and fourth generation methods, including their robustness to misspecification of priors in the analysis of large phylogenies and data sets.

Tree of life reveals clock-like speciation and diversification.

Genomic data are rapidly resolving the tree of living species calibrated to time, the timetree of life, which will provide a framework for research in diverse fields of science. Previous analyses of taxonomically restricted timetrees have found a decline in the rate of diversification in many groups of organisms, often attributed to ecological interactions among species. Here, we have synthesized a global timetree of life from 2,274 studies representing 50,632 species and examined the pattern and rate of diversification as well as the timing of speciation. We found that species diversity has been mostly expanding overall and in many smaller groups of species, and that the rate of diversification in eukaryotes has been mostly constant. We also identified, and avoided, potential biases that may have influenced previous analyses of diversification including low levels of taxon sampling, small clade size, and the inclusion of stem branches in clade analyses. We found consistency in time-to-speciation among plants and animals, ∼2 My, as measured by intervals of crown and stem species times. Together, this clock-like change at different levels suggests that speciation and diversification are processes dominated by random events and that adaptive change is largely a separate process.

Discovery of a Giant Chameleon-Like Lizard (Anolis) on Hispaniola and Its Significance to Understanding Replicated Adaptive Radiations.

We report a new chameleon-like Anolis species from Hispaniola that is ecomorphologically similar to congeners found only on Cuba. Lizards from both clades possess short limbs and a short tail and utilize relatively narrow perches, leading us to recognize a novel example of ecomorphological matching among islands in the well-known Greater Antillean anole radiation. This discovery supports the hypothesis that the assembly of island faunas can be substantially deterministic and highlights the continued potential for basic discovery to reveal new insights in well-studied groups. Restricted to a threatened band of midelevation transitional forest near the border of the Dominican Republic and Haiti, this new species appears to be highly endangered.

Global mammal beta diversity shows parallel assemblage structure in similar but isolated environments.

The taxonomic, phylogenetic and trait dimensions of beta diversity each provide us unique insights into the importance of historical isolation and environmental conditions in shaping global diversity. These three dimensions should, in general, be positively correlated. However, if similar environmental conditions filter species with similar trait values, then assemblages located in similar environmental conditions, but separated by large dispersal barriers, may show high taxonomic, high phylogenetic, but low trait beta diversity. Conversely, we expect lower phylogenetic diversity, but higher trait biodiversity among assemblages that are connected but are in differing environmental conditions. We calculated all pairwise comparisons of approximately 110 × 110 km grid cells across the globe for more than 5000 mammal species (approx. 70 million comparisons). We considered realms as units representing geographical distance and historical isolation and biomes as units with similar environmental conditions. While beta diversity dimensions were generally correlated, we highlight geographical regions of decoupling among beta diversity dimensions. Our analysis shows that assemblages from tropical forests in different realms had low trait dissimilarity while phylogenetic beta diversity was significantly higher than expected, suggesting potential convergent evolution. Low trait beta diversity was surprisingly not found between isolated deserts, despite harsh environmental conditions. Overall, our results provide evidence for parallel assemblage structure of mammal assemblages driven by environmental conditions at a global scale.

Methodological congruence in phylogenomic analyses with morphological support for teiid lizards (Sauria: Teiidae).

A well-known issue in phylogenetics is discordance among gene trees, species trees, morphology, and other data types. Gene-tree discordance is often caused by incomplete lineage sorting, lateral gene transfer, and gene duplication. Multispecies-coalescent methods can account for incomplete lineage sorting and are believed by many to be more accurate than concatenation. However, simulation studies and empirical data have demonstrated that concatenation and species tree methods often recover similar topologies. We use three popular methods of phylogenetic reconstruction (one concatenation, two species tree) to evaluate relationships within Teiidae. These lizards are distributed across the United States to Argentina and the West Indies, and their classification has been controversial due to incomplete sampling and the discordance among various character types (chromosomes, DNA, musculature, osteology, etc.) used to reconstruct phylogenetic relationships. Recent morphological and molecular analyses of the group resurrected three genera and created five new genera to resolve non-monophyly in three historically ill-defined genera: Ameiva, Cnemidophorus, and Tupinambis. Here, we assess the phylogenetic relationships of the Teiidae using "next-generation" anchored-phylogenomics sequencing. Our final alignment includes 316 loci (488,656bp DNA) for 244 individuals (56 species of teiids, representing all currently recognized genera) and all three methods (ExaML, MP-EST, and ASTRAL-II) recovered essentially identical topologies. Our results are basically in agreement with recent results from morphology and smaller molecular datasets, showing support for monophyly of the eight new genera. Interestingly, even with hundreds of loci, the relationships among some genera in Tupinambinae remain ambiguous (i.e. low nodal support for the position of Salvator and Dracaena).