Increasing the impact of vertebrate scientific collections through 3D imaging: The openVertebrate (oVert) Thematic Collections Network.

The impact of preserved museum specimens is transforming and increasing by three-dimensional (3D) imaging that creates high-fidelity online digital specimens. Through examples from the openVertebrate (oVert) Thematic Collections Network, we describe how we created a digitization community dedicated to the shared vision of making 3D data of specimens available and the impact of these data on a broad audience of scientists, students, teachers, artists, and more. High-fidelity digital 3D models allow people from multiple communities to simultaneously access and use scientific specimens. Based on our multiyear, multi-institution project, we identify significant technological and social hurdles that remain for fully realizing the potential impact of digital 3D specimens.

The macroevolutionary singularity of snakes.

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.

Ecological correlates of cranial evolution in the megaradiation of dipsadine snakes.

BACKGROUND: Dipsadine snakes represent one of the most spectacular vertebrate radiations that have occurred in any continental setting, with over 800 species in South and Central America. Their species richness is paralleled by stunning ecological diversity, ranging from arboreal snail-eating and aquatic eel-eating specialists to terrestrial generalists. Despite the ecological importance of this clade, little is known about the extent to which ecological specialization shapes broader patterns of phenotypic diversity within the group. Here, we test how habitat use and diet have influenced morphological diversification in skull shape across 160 dipsadine species using micro-CT and 3-D geometric morphometrics, and we use a phylogenetic comparative approach to test the contributions of habitat use and diet composition to variation in skull shape among species. RESULTS: We demonstrate that while both habitat use and diet are significant predictors of shape in many regions of the skull, habitat use significantly predicts shape in a greater number of skull regions when compared to diet. We also find that across ecological groupings, fossorial and aquatic behaviors result in the strongest deviations in morphospace for several skull regions. We use simulations to address the robustness of our results and describe statistical anomalies that can arise from the application of phylogenetic generalized least squares to complex shape data. CONCLUSIONS: Both habitat and dietary ecology are significantly correlated with skull shape in dipsadines; the strongest relationships involved skull shape in snakes with aquatic and fossorial lifestyles. This association between skull morphology and multiple ecological axes is consistent with a classic model of adaptive radiation and suggests that ecological factors were an important component in driving morphological diversification in the dipsadine megaradiation.

Notes from the taxonomic disaster zone: Evolutionary drivers of intractable species boundaries in an Australian lizard clade (Scincidae: Ctenotus).

Genomic-scale datasets, sophisticated analytical techniques, and conceptual advances have disproportionately failed to resolve species boundaries in some groups relative to others. To understand the processes that underlie taxonomic intractability, we dissect the speciation history of an Australian lizard clade that arguably represents a "worst-case" scenario for species delimitation within vertebrates: the Ctenotus inornatus species group, a clade beset with decoupled genetic and phenotypic breaks, uncertain geographic ranges, and parallelism in purportedly diagnostic morphological characters. We sampled hundreds of localities to generate a genomic perspective on population divergence, structure, and admixture. Our results revealed rampant paraphyly of nominate taxa in the group, with lineages that are either morphologically cryptic or polytypic. Isolation-by-distance patterns reflect spatially continuous differentiation among certain pairs of putative species, yet genetic and geographic distances are decoupled in other pairs. Comparisons of mitochondrial and nuclear gene trees, tests of nuclear introgression, and historical demographic modelling identified gene flow between divergent candidate species. Levels of admixture are decoupled from phylogenetic relatedness; gene flow is often higher between sympatric species than between parapatric populations of the same species. Such idiosyncratic patterns of introgression contribute to species boundaries that are fuzzy while also varying in fuzziness. Our results suggest that "taxonomic disaster zones" like the C. inornatus species group result from spatial variation in the porosity of species boundaries and the resulting patterns of genetic and phenotypic variation. This study raises questions about the origin and persistence of hybridizing species and highlights the unique insights provided by taxa that have long eluded straightforward taxonomic categorization.

Diversification dynamics in Caribbean rain frogs (Eleutherodactylus) are uncoupled from the anuran community and consistent with adaptive radiation.

Adaptive radiation is proposed to play a key role in generating differences in species richness among lineages and geographical regions. Due to the importance of ecological divergence in adaptive radiation, species richness is predicted to be influenced by equilibrium diversity dynamics, although the concept continues to generate much debate. An additional important question is whether radiating clades have intrinsic biological characteristics that make them particularly prone to diversify. We tackle these questions by analysing (i) the temporal patterns of diversification of Caribbean Eleutherodactylus frogs, and (ii) assembly of the complete native anuran community of the Caribbean archipelago (197 species), testing for the presence of equilibrium dynamics and whether diversification patterns of Eleutherodactylus differ from those of the rest of the Caribbean anurans. Diversification rates follow the predicted pattern of rapid diversification early in the radiation which gradually decreases towards the present. Eleutherodactylus diversification is significantly faster than that of the Caribbean anuran community, and although equilibrium dynamics influence richness of all Caribbean anurans, Eleutherodactylus shows higher carrying capacity. Our results indicate that ecological opportunity per se is not sufficient for adaptive radiation and that diverse lineages present intrinsic characteristics that enable them to make the most of available opportunity.

Assembling microbial communities: a genomic analysis of a natural experiment in neotropical bamboo internodes.

Microbes participate in ecological communities, much like multicellular organisms. However, microbial communities lack the centuries of observation and theory describing and predicting ecological processes available for multicellular organisms. Here, we examine early bacterial community assembly in the water-filled internodes of Amazonian bamboos from the genus Guadua. Bamboo stands form distinct habitat patches within the lowland Amazonian rainforest and provide habitat for a suite of vertebrate and invertebrate species. Guadua bamboos develop sealed, water-filled internodes as they grow. Internodes are presumed sterile or near sterile while closed, but most are eventually opened to the environment by animals, after which they are colonized by microbes. We find that microbial community diversity increases sharply over the first few days of environmental exposure, and taxonomic identity of the microbes changes through this time period as is predicted for early community assembly in macroscopic communities. Microbial community taxonomic turnover is consistent at the bacteria phylum level, but at the level of Operational Taxonomic Units (OTUs), internode communities become increasingly differentiated through time. We argue that these tropical bamboos form an ideal study system for microbial community ecology due to their near-sterile condition prior to opening, relatively consistent environment after opening, and functionally limitless possibilities for replicates. Given the possible importance of opened internode habitats as locations of transmission for both pathogenic and beneficial microbes among animals, understanding the microbial dynamics of the internode habitat is a key conservation concern for the insect and amphibian species that use this microhabitat.

Evolutionary time and species diversity in aquatic ecosystems worldwide.

The latitudinal diversity gradient (LDG) is frequently described as the most dramatic biodiversity pattern on Earth, yet ecologists and biogeographers have failed to reach consensus on its primary cause. A key problem in explaining the LDG involves collinearity between multiple factors that are predicted to affect species richness in the same direction. In terrestrial systems, energy input, geographic area, and evolutionary time for species accumulation tend to covary positively with species richness at the largest spatial scales, such that their individual contributions to the LDG are confounded in global analyses. I review three diversity patterns from marine and freshwater systems that break this collinearity and which may thus provide stronger tests of the influence of time on global richness gradients. Specifically, I contrast biodiversity patterns along oceanic depth gradients, in geologically young versus ancient lakes, and in the north versus south polar marine biomes. I focus primarily on fishes due to greater data availability but synthesize patterns for invertebrates where possible. I find that regional-to-global species richness generally declines with depth in the oceans, despite the great age and stability of the deep-sea biome. Geologically ancient lakes generally do not contain more species than young lakes, and the Antarctic marine biome is not appreciably more species rich than the much younger Arctic marine biome. However, endemism is consistently higher in older systems. Patterns for invertebrate groups are less clear than for fishes and reflect a critical need for primary biodiversity data. In summary, the available data suggest that species richness is either decoupled from or only weakly related to the amount of time for diversification. These results suggest that energy, productivity, or geographic area are the primary drivers of large-scale diversity gradients. To the extent that marine and terrestrial diversity gradients result from similar processes, these examples provide evidence against a primary role for evolutionary time as the cause of the LDG.

Genetic variability and the ecology of geographic range: A test of the central-marginal hypothesis in Australian scincid lizards.

For many species, both local abundance and regional occupancy are highest near the centre of their geographic distributions. One hypothesis for this pattern is that niche suitability declines with increasing distance from a species geographic centre, such that populations near range margins are characterized by reduced density and increased patchiness. In these smaller edge populations, genetic drift is more powerful, leading to the loss of genetic diversity. This simple verbal model has been formalized as the central-marginal hypothesis, which predicts that core populations should have greater genetic diversity than edge populations. Here, we tested the central-marginal hypothesis using a genomic data set of 25 species-level taxa of Australian scincid lizards in the genera Ctenotus and Lerista. A majority of taxa in our data set showed range-wide patterns of genetic variation consistent with central-marginal hypothesis, and eight of 25 taxa showed significantly greater genetic diversity in the centre of their range. We then explored biological, historical, and methodological factors that might predict which taxa support the central-marginal hypothesis. We found that taxa with the strongest evidence for range expansion were the least likely to follow predictions of the central-marginal hypothesis. The majority of these taxa had range expansions that originated at the range edge, which led to a gradient of decreasing genetic diversity from the range edge to the core, contrary to the central-marginal hypothesis.

Fast Likelihood Calculations for Automatic Identification of Macroevolutionary Rate Heterogeneity in Continuous and Discrete Traits.

Understanding phenotypic disparity across the tree of life requires identifying where and when evolutionary rates change on phylogeny. A primary methodological challenge in macroevolution is therefore to develop methods for accurate inference of among-lineage variation in rates of phenotypic evolution. Here, we describe a method for inferring among-lineage evolutionary rate heterogeneity in both continuous and discrete traits. The method assumes that the present-day distribution of a trait is shaped by a variable-rate process arising from a mixture of constant-rate processes and uses a single-pass tree traversal algorithm to estimate branch-specific evolutionary rates. By employing dynamic programming optimization techniques and approximate maximum likelihood estimators where appropriate, our method permits rapid exploration of the tempo and mode of phenotypic evolution. Simulations indicate that the method reconstructs rates of trait evolution with high accuracy. Application of the method to data sets on squamate reptile reproduction and turtle body size recovers patterns of rate heterogeneity identified by previous studies but with computational costs reduced by many orders of magnitude. Our results expand the set of tools available for detecting macroevolutionary rate heterogeneity and point to the utility of fast, approximate methods for studying large-scale biodiversity dynamics. [Brownian motion; continuous characters; discrete characters; macroevolution; Markov process; rate heterogeneity.].

Genetic and Ecogeographic Controls on Species Cohesion in Australia's Most Diverse Lizard Radiation.

AbstractSpecies vary extensively in geographic range size and climatic niche breadth. If range limits are primarily determined by climatic factors, species with broad climatic tolerances and those that track geographically widespread climates should have large ranges. However, large ranges might increase the probability of population fragmentation and adaptive divergence, potentially decoupling climatic niche breadth and range size. Conversely, ecological generalism in large-ranged species might lead to higher gene flow across climatic transitions, increasing species' cohesion and thus decreasing genetic isolation by distance (IBD). Focusing on Australia's iconic Ctenotus lizard radiation, we ask whether species range size scales with climatic niche breadth and the degree of population isolation. To this end, we infer independently evolving operational taxonomic units (OTUs), their geographic and climatic ranges, and the strength of IBD within OTUs based on genome-wide loci from 722 individuals spanning 75 taxa. Large-ranged OTUs were common and had broader climatic niches than small-ranged OTUs; thus, large ranges do not appear to simply result from passive tracking of widespread climatic zones. OTUs with larger ranges and broader climatic niches showed relatively weaker IBD, suggesting that large-ranged species might possess intrinsic attributes that facilitate genetic cohesion across large distances and varied climates. By influencing population divergence and persistence, traits that affect species cohesion may play a central role in large-scale patterns of diversification and species richness.

No link between population isolation and speciation rate in squamate reptiles.

Rates of species formation vary widely across the tree of life and contribute to massive disparities in species richness among clades. This variation can emerge from differences in metapopulation-level processes that affect the rates at which lineages diverge, persist, and evolve reproductive barriers and ecological differentiation. For example, populations that evolve reproductive barriers quickly should form new species at faster rates than populations that acquire reproductive barriers more slowly. This expectation implicitly links microevolutionary processes (the evolution of populations) and macroevolutionary patterns (the profound disparity in speciation rate across taxa). Here, leveraging extensive field sampling from the Neotropical Cerrado biome in a biogeographically controlled natural experiment, we test the role of an important microevolutionary process-the propensity for population isolation-as a control on speciation rate in lizards and snakes. By quantifying population genomic structure across a set of codistributed taxa with extensive and phylogenetically independent variation in speciation rate, we show that broad-scale patterns of species formation are decoupled from demographic and genetic processes that promote the formation of population isolates. Population isolation is likely a critical stage of speciation for many taxa, but our results suggest that interspecific variability in the propensity for isolation has little influence on speciation rates. These results suggest that other stages of speciation-including the rate at which reproductive barriers evolve and the extent to which newly formed populations persist-are likely to play a larger role than population isolation in controlling speciation rate variation in squamates.

Biodiversity across space and time in the fossil record.

The fossil record is the primary source of information on how biodiversity has varied in deep time, providing unique insight on the long-term dynamics of diversification and their drivers. However, interpretations of fossil record diversity patterns have been much debated, with a traditional focus on global diversity through time. Problems arise because the fossil record is spatially and temporally patchy, so 'global' diversity estimates actually represent the summed diversity across a set of geographically and environmentally distinct regions that vary substantially in number and identity through time. Furthermore, a focus on global diversity lumps the signal of ecological drivers at local and regional scales with the signal of global-scale processes, including variation in the distribution of environments and in provincialism (the extent of subdivision into distinct biogeographic regions). These signals cannot be untangled by studying global diversity measures alone. These conceptual and empirical concerns necessitate a shift away from the study of 'biodiversity through time' and towards the study of 'biodiversity across time and space'. Spatially explicit investigations, including analyses of local- and regional-scale datasets, are central to achieving this and allow analysis of geographic scale, location and the environmental parameters directly experienced by organisms. So far, research in this area has revealed the stability of species richness variation among environments through time, and the potential climatic and Earth-system drivers of changing biodiversity. Ultimately, this research program promises to address key questions regarding the assembly of biodiversity, and the contributions of local-, regional- and global-scale processes to the diversification of life on Earth.

Rapid increase in snake dietary diversity and complexity following the end-Cretaceous mass extinction.

The Cenozoic marked a period of dramatic ecological opportunity in Earth history due to the extinction of non-avian dinosaurs as well as to long-term physiographic changes that created new biogeographic theaters and new habitats. Snakes underwent massive ecological diversification during this period, repeatedly evolving novel dietary adaptations and prey preferences. The evolutionary tempo and mode of these trophic ecological changes remain virtually unknown, especially compared with co-radiating lineages of birds and mammals that are simultaneously predators and prey of snakes. Here, we assemble a dataset on snake diets (34,060 observations on the diets of 882 species) to investigate the history and dynamics of the multidimensional trophic niche during the global radiation of snakes. Our results show that per-lineage dietary niche breadths remained remarkably constant even as snakes diversified to occupy disparate outposts of dietary ecospace. Rapid increases in dietary diversity and complexity occurred in the early Cenozoic, and the overall rate of ecospace expansion has slowed through time, suggesting a potential response to ecological opportunity in the wake of the end-Cretaceous mass extinction. Explosive bursts of trophic innovation followed colonization of the Nearctic and Neotropical realms by a group of snakes that today comprises a majority of living snake diversity. Our results indicate that repeated transformational shifts in dietary ecology are important drivers of adaptive radiation in snakes and provide a framework for analyzing and visualizing the evolution of complex ecological phenotypes on phylogenetic trees.

Macroevolutionary thermodynamics: Temperature and the tempo of evolution in the tropics.

An influential hypothesis proposes that the tempo of evolution is faster in the tropics. Emerging evidence, including a study in this issue of PLOS Biology, challenges this view, raising new questions about the causes of Earth's iconic latitudinal diversity gradient (LDG).

A return-on-investment approach for prioritization of rigorous taxonomic research needed to inform responses to the biodiversity crisis.

Global biodiversity loss is a profound consequence of human activity. Disturbingly, biodiversity loss is greater than realized because of the unknown number of undocumented species. Conservation fundamentally relies on taxonomic recognition of species, but only a fraction of biodiversity is described. Here, we provide a new quantitative approach for prioritizing rigorous taxonomic research for conservation. We implement this approach in a highly diverse vertebrate group-Australian lizards and snakes. Of 870 species assessed, we identified 282 (32.4%) with taxonomic uncertainty, of which 17.6% likely comprise undescribed species of conservation concern. We identify 24 species in need of immediate taxonomic attention to facilitate conservation. Using a broadly applicable return-on-investment framework, we demonstrate the importance of prioritizing the fundamental work of identifying species before they are lost.

Ecological and biogeographic drivers of biodiversity cannot be resolved using clade age-richness data.

Estimates of evolutionary diversification rates - speciation and extinction - have been used extensively to explain global biodiversity patterns. Many studies have analyzed diversification rates derived from just two pieces of information: a clade's age and its extant species richness. This "age-richness rate" (ARR) estimator provides a convenient shortcut for comparative studies, but makes strong assumptions about the dynamics of species richness through time. Here we demonstrate that use of the ARR estimator in comparative studies is problematic on both theoretical and empirical grounds. We prove mathematically that ARR estimates are non-identifiable: there is no information in the data for a single clade that can distinguish a process with positive net diversification from one where net diversification is zero. Using paleontological time series, we demonstrate that the ARR estimator has no predictive ability for real datasets. These pathologies arise because the ARR inference procedure yields "point estimates" that have been computed under a saturated statistical model with zero degrees of freedom. Although ARR estimates remain useful in some contexts, they should be avoided for comparative studies of diversification and species richness.

A test for rate-coupling of trophic and cranial evolutionary dynamics in New World bats.

Morphological evolution is often assumed to be causally related to underlying patterns of ecological trait evolution. However, few studies have directly tested whether evolutionary dynamics of-and major shifts in-ecological resource use are coupled with morphological shifts that may facilitate trophic innovation. Using diet and multivariate cranial (microCT) data, we tested whether rates of trophic and cranial evolution are coupled in the radiation of New World bats. We developed a generalizable information-theoretic method for describing evolutionary rate heterogeneity across large candidate sets of multirate evolutionary models, without relying on a single best-fitting model. We found considerable variation in trophic evolutionary dynamics, in sharp contrast to a largely homogeneous cranial evolutionary process. This dichotomy is surprising given established functional associations between overall skull morphology and trophic ecology. We suggest that assigning discrete trophic states may underestimate trophic generalism and opportunism, and that this radiation could be characterized by labile crania and a homogeneous dynamic of generally high morphological rates. Overall, we discuss how trophic classifications could substantively impact our interpretation of how these dynamics covary in adaptive radiations.

Detecting Lineage-Specific Shifts in Diversification: A Proper Likelihood Approach.

The branching patterns of molecular phylogenies are generally assumed to contain information on rates of the underlying speciation and extinction processes. Simple birth-death models with constant, time-varying, or diversity-dependent rates have been invoked to explain these patterns. They have one assumption in common: all lineages have the same set of diversification rates at a given point in time. It seems likely, however, that there is variability in diversification rates across subclades in a phylogenetic tree. This has inspired the construction of models that allow multiple rate regimes across the phylogeny, with instantaneous shifts between these regimes. Several methods exist for calculating the likelihood of a phylogeny under a specified mapping of diversification regimes and for performing inference on the most likely diversification history that gave rise to a particular phylogenetic tree. Here, we show that the likelihood computation of these methods is not correct. We provide a new framework to compute the likelihood correctly and show, with simulations of a single shift, that the correct likelihood indeed leads to parameter estimates that are on average in much better agreement with the generating parameters than the incorrect likelihood. Moreover, we show that our corrected likelihood can be extended to multiple rate shifts in time-dependent and diversity-dependent models. We argue that identifying shifts in diversification rates is a nontrivial model selection exercise where one has to choose whether shifts in now-extinct lineages are taken into account or not. Hence, our framework also resolves the recent debate on such unobserved shifts. [Diversification; macroevolution; phylogeny; speciation].

Congruence and Conflict in the Higher-Level Phylogenetics of Squamate Reptiles: An Expanded Phylogenomic Perspective.

Genome-scale data have the potential to clarify phylogenetic relationships across the tree of life but have also revealed extensive gene tree conflict. This seeming paradox, whereby larger data sets both increase statistical confidence and uncover significant discordance, suggests that understanding sources of conflict is important for accurate reconstruction of evolutionary history. We explore this paradox in squamate reptiles, the vertebrate clade comprising lizards, snakes, and amphisbaenians. We collected an average of 5103 loci for 91 species of squamates that span higher-level diversity within the clade, which we augmented with publicly available sequences for an additional 17 taxa. Using a locus-by-locus approach, we evaluated support for alternative topologies at 17 contentious nodes in the phylogeny. We identified shared properties of conflicting loci, finding that rate and compositional heterogeneity drives discordance between gene trees and species tree and that conflicting loci rarely overlap across contentious nodes. Finally, by comparing our tests of nodal conflict to previous phylogenomic studies, we confidently resolve 9 of the 17 problematic nodes. We suggest this locus-by-locus and node-by-node approach can build consensus on which topological resolutions remain uncertain in phylogenomic studies of other contentious groups. [Anchored hybrid enrichment (AHE); gene tree conflict; molecular evolution; phylogenomic concordance; target capture; ultraconserved elements (UCE).].

What makes a fang? Phylogenetic and ecological controls on tooth evolution in rear-fanged snakes.

BACKGROUND: Fangs are a putative key innovation that revolutionized prey capture and feeding in snakes, and - along with their associated venom phenotypes - have made snakes perhaps the most medically-significant vertebrate animals. Three snake clades are known for their forward-positioned fangs, and these clades (Elapidae, Viperidae, and Atractaspidinae) contain the majority of snakes that are traditionally considered venomous. However, many other snakes are "rear-fanged": they possess potentially venom-delivering teeth situated at the rear end of the upper jaw. Quantification of fang phenotypes - and especially those of rear-fanged species - has proved challenging or impossible owing to the small size and relative rarity of many such snakes. Consequently, it has been difficult to understand the evolutionary history of both venom and prey-capture strategies across extant snakes. We quantified variation in the dentition of 145 colubriform ("advanced") snake species using microCT scanning and compared dental characters with ecological data on species' diet and prey capture method(s) to understand broader patterns in snake fang evolution. RESULTS: Dental traits such as maxilla length, tooth number, and fang size show strong phylogenetic signal across Colubriformes. We find extreme heterogeneity and evolutionary lability in the rear-fanged phenotype in colubrid (colubrine, dipsadine, and natricine lineages) and lamprophiid snakes, in contrast to relative uniformity in the front fanged phenotypes of other groups (vipers and, to a lesser extent, elapids). Fang size and position are correlated with venom-use in vipers, elapids, and colubrid snakes, with the latter group shifting fangs anteriorly by shortening the entire maxillary bone. We find that maxilla length and tooth number may also be correlated with the evolution of dietary specialization. Finally, an ancestral state reconstruction suggests that fang loss is a recurring phenomenon in colubrid snakes, likely accompanied by shifts in diet and prey capture mode. CONCLUSIONS: Our study provides a framework for quantifying the complex morphologies associated with venom use in snakes. Our results suggest that fang phenotypes, and particularly the rear-fanged phenotype, in snakes are both diverse and labile, facilitating a wide range of ecological strategies and contributing to spectacular radiations of these organisms in tropical and subtropical biomes worldwide.