Trophically integrated ecometric models as tools for demonstrating spatial and temporal functional changes in mammal communities.

We are in a modern biodiversity crisis that will restructure community compositions and ecological functions globally. Large mammals, important contributors to ecosystem function, have been affected directly by purposeful extermination and indirectly by climate and land-use changes, yet functional turnover is rarely assessed on a global scale using metrics based on functional traits. Using ecometrics, the study of functional trait distributions and functional turnover, we examine the relationship between vegetation cover and locomotor traits for artiodactyl and carnivoran communities. We show that the ability to detect a functional relationship is strengthened when locomotor traits of both primary consumers (artiodactyls, n = 157 species) and secondary consumers (carnivorans, n = 138 species) are combined into one trophically integrated ecometric model. Overall, locomotor traits of 81% of communities accurately estimate vegetation cover, establishing the advantage of trophically integrated ecometric models over single-group models (58 to 65% correct). We develop an innovative approach within the ecometrics framework, using ecometric anomalies to evaluate mismatches in model estimates and observed values and provide more nuance for understanding relationships between functional traits and vegetation cover. We apply our integrated model to five paleontological sites to illustrate mismatches in the past and today and to demonstrate the utility of the model for paleovegetation interpretations. Observed changes in community traits and their associated vegetations across space and over time demonstrate the strong, rapid effect of environmental filtering on community traits. Ultimately, our trophically integrated ecometric model captures the cascading interactions between taxa, traits, and changing environments.

Measuring mantled howler monkey (Alouatta palliata) testes via parallel laser photogrammetry: Expanding the use of noninvasive methods.

Parallel laser photogrammetry (PLP), which consists of attaching two or three parallel laser beams at a known inter-beam distance to a camera, can be used to collect morphological measurements of organisms noninvasively. The lasers project onto the photo being taken, and because the inter-beam distance is known, they act as a scale for image analysis programs like ImageJ. Traditionally, this method has been used to measure larger morphological traits (e.g., limb length, crown-rump length) to serve as proxies for overall body size, whereas applications to smaller anatomical features remain limited. To that end, we used PLP to measure the testes of 18 free-living mantled howler monkeys (Alouatta palliata) at La Selva Biological Station, Costa Rica. We tested whether this method could reliably measure this relatively small and globular morphology, and whether it could detect differences among individuals. We tested reliability in three ways: within-photo (coefficient of variation [CV] = 4.7%), between-photo (CV = 5.5%), and interobserver (intraclass correlation = 0.92). We found an average volume of 36.2 cm3 and a range of 16.4-54.4 cm3, indicating variation in testes size between individuals. Furthermore, these sizes are consistent with a previous study that collected measurements by hand, suggesting that PLP is a useful method for making noninvasive measurements of testes.

On Information Rank Deficiency in Phenotypic Covariance Matrices.

This article investigates a form of rank deficiency in phenotypic covariance matrices derived from geometric morphometric data, and its impact on measures of phenotypic integration. We first define a type of rank deficiency based on information theory then demonstrate that this deficiency impairs the performance of phenotypic integration metrics in a model system. Lastly, we propose methods to treat for this information rank deficiency. Our first goal is to establish how the rank of a typical geometric morphometric covariance matrix relates to the information entropy of its eigenvalue spectrum. This requires clear definitions of matrix rank, of which we define three: the full matrix rank (equal to the number of input variables), the mathematical rank (the number of nonzero eigenvalues), and the information rank or "effective rank" (equal to the number of nonredundant eigenvalues). We demonstrate that effective rank deficiency arises from a combination of methodological factors-Generalized Procrustes analysis, use of the correlation matrix, and insufficient sample size-as well as phenotypic covariance. Secondly, we use dire wolf jaws to document how differences in effective rank deficiency bias two metrics used to measure phenotypic integration. The eigenvalue variance characterizes the integration change incorrectly, and the standardized generalized variance lacks the sensitivity needed to detect subtle changes in integration. Both metrics are impacted by the inclusion of many small, but nonzero, eigenvalues arising from a lack of information in the covariance matrix, a problem that usually becomes more pronounced as the number of landmarks increases. We propose a new metric for phenotypic integration that combines the standardized generalized variance with information entropy. This metric is equivalent to the standardized generalized variance but calculated only from those eigenvalues that carry nonredundant information. It is the standardized generalized variance scaled to the effective rank of the eigenvalue spectrum. We demonstrate that this metric successfully detects the shift of integration in our dire wolf sample. Our third goal is to generalize the new metric to compare data sets with different sample sizes and numbers of variables. We develop a standardization for matrix information based on data permutation then demonstrate that Smilodon jaws are more integrated than dire wolf jaws. Finally, we describe how our information entropy-based measure allows phenotypic integration to be compared in dense semilandmark data sets without bias, allowing characterization of the information content of any given shape, a quantity we term "latent dispersion". [Canis dirus; Dire wolf; effective dispersion; effective rank; geometric morphometrics; information entropy; latent dispersion; modularity and integration; phenotypic integration; relative dispersion.].

Evolution of the snake body form reveals homoplasy in amniote Hox gene function.

Hox genes regulate regionalization of the axial skeleton in vertebrates, and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms. The origin of the snake-like body form, with its deregionalized pre-cloacal axial skeleton, has been explained as either homogenization of Hox gene expression domains, or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions. Both models assume a highly regionalized ancestor, but the extent of deregionalization of the primaxial domain (vertebrae, dorsal ribs) of the skeleton in snake-like body forms has never been analysed. Here we combine geometric morphometrics and maximum-likelihood analysis to show that the pre-cloacal primaxial domain of elongate, limb-reduced lizards and snakes is not deregionalized compared with limbed taxa, and that the phylogenetic structure of primaxial morphology in reptiles does not support a loss of regionalization in the evolution of snakes. We demonstrate that morphometric regional boundaries correspond to mapped gene expression domains in snakes, suggesting that their primaxial domain is patterned by a normally functional Hox code. Comparison of primaxial osteology in fossil and modern amniotes with Hox gene distributions within Amniota indicates that a functional, sequentially expressed Hox code patterned a subtle morphological gradient along the anterior-posterior axis in stem members of amniote clades and extant lizards, including snakes. The highly regionalized skeletons of extant archosaurs and mammals result from independent evolution in the Hox code and do not represent ancestral conditions for clades with snake-like body forms. The developmental origin of snakes is best explained by decoupling of the primaxial and abaxial domains and by increases in somite number, not by changes in the function of primaxial Hox genes.

Is the middle cranial fossa a reliable predictor of temporal lobe volume in extant and fossil anthropoids?

OBJECTIVES: We investigate the suitability of middle cranial fossa (MCF) size as a proxy for temporal lobe volume (TLV), examining the strength of the association between TLV and MCF metrics and assess the reliability predicting TLV in fossil anthropoids. The temporal lobe of the primate brain is a multimodal association cortex involved in long-term memory, auditory, and visual processing with unique specializations in modern humans for language comprehension. The MCF is the bony counterpart for the temporal lobe providing inferences for fossil hominin temporal lobe evolution. We now investigate whether the MCF is a suitable proxy for the temporal lobe. METHODS: A sample of 23 anthropoid species (n = 232, including 13 fossil species) from computed tomography (CT) scans of ex vivo crania and magnetic resonance imaging (MRI) of the in vivo brain were generated into three-dimensional (3D) virtual models. Seven linear metrics were digitally measured on the right MCF with right TLV calculated from in vivo MRI. RESULTS: Regression analyses produced statistically significant correlations between TLV and all MCF metrics (r ≥ 0.85; p ≤ 0.0009) with TLV predictions within ±1 standard error and three MCF metrics (posterior-width, mid-length, and mid-width) the most reliable predictors of TLV with only one metric weakly associated with TLV. DISCUSSION: These findings indicate a strong association between the MCF and TLV, provide reliable predictors of fossil TLV that were previously unattainable, allow the inclusion of fragmentary fossil material, and enable inferences into the emergence of modern human temporal lobe morphology.

Brain enlargement and dental reduction were not linked in hominin evolution.

The large brain and small postcanine teeth of modern humans are among our most distinctive features, and trends in their evolution are well studied within the hominin clade. Classic accounts hypothesize that larger brains and smaller teeth coevolved because behavioral changes associated with increased brain size allowed a subsequent dental reduction. However, recent studies have found mismatches between trends in brain enlargement and posterior tooth size reduction in some hominin species. We use a multiple-variance Brownian motion approach in association with evolutionary simulations to measure the tempo and mode of the evolution of endocranial and dental size and shape within the hominin clade. We show that hominin postcanine teeth have evolved at a relatively consistent neutral rate, whereas brain size evolved at comparatively more heterogeneous rates that cannot be explained by a neutral model, with rapid pulses in the branches leading to later Homo species. Brain reorganization shows evidence of elevated rates only much later in hominin evolution, suggesting that fast-evolving traits such as the acquisition of a globular shape may be the result of direct or indirect selection for functional or structural traits typical of modern humans.

Including Fossils in Phylogenetic Climate Reconstructions: A Deep Time Perspective on the Climatic Niche Evolution and Diversification of Spiny Lizards (Sceloporus).

Fossils and other paleontological information can improve phylogenetic comparative method estimates of phenotypic evolution and generate hypotheses related to species diversification. Here, we use fossil information to calibrate ancestral reconstructions of suitable climate for Sceloporus lizards in North America. Integrating data from the fossil record, general circulation models of paleoclimate during the Miocene, climate envelope modeling, and phylogenetic comparative methods provides a geographically and temporally explicit species distribution model of Sceloporus-suitable habitat through time. We provide evidence to support the historic biogeographic hypothesis of Sceloporus diversification in warm North American deserts and suggest a relatively recent Sceloporus invasion into Mexico around 6 Ma. We use a physiological model to map extinction risk. We suggest that the number of hours of restriction to a thermal refuge limited Sceloporus from inhabiting Mexico until the climate cooled enough to provide suitable habitat at approximately 6 Ma. If the future climate returns to the hotter climates of the past, Mexico, the place of highest modern Sceloporus richness, will no longer provide suitable habitats for Sceloporus to survive and reproduce.

The Fossil Calibration Database-A New Resource for Divergence Dating.

Fossils provide the principal basis for temporal calibrations, which are critical to the accuracy of divergence dating analyses. Translating fossil data into minimum and maximum bounds for calibrations is the most important-often least appreciated-step of divergence dating. Properly justified calibrations require the synthesis of phylogenetic, paleontological, and geological evidence and can be difficult for nonspecialists to formulate. The dynamic nature of the fossil record (e.g., new discoveries, taxonomic revisions, updates of global or local stratigraphy) requires that calibration data be updated continually lest they become obsolete. Here, we announce the Fossil Calibration Database (http://fossilcalibrations.org), a new open-access resource providing vetted fossil calibrations to the scientific community. Calibrations accessioned into this database are based on individual fossil specimens and follow best practices for phylogenetic justification and geochronological constraint. The associated Fossil Calibration Series, a calibration-themed publication series at Palaeontologia Electronica, will serve as a key pipeline for peer-reviewed calibrations to enter the database.

No known hominin species matches the expected dental morphology of the last common ancestor of Neanderthals and modern humans.

A central problem in paleoanthropology is the identity of the last common ancestor of Neanderthals and modern humans ([N-MH]LCA). Recently developed analytical techniques now allow this problem to be addressed using a probabilistic morphological framework. This study provides a quantitative reconstruction of the expected dental morphology of the [N-MH]LCA and an assessment of whether known fossil species are compatible with this ancestral position. We show that no known fossil species is a suitable candidate for being the [N-MH]LCA and that all late Early and Middle Pleistocene taxa from Europe have Neanderthal dental affinities, pointing to the existence of a European clade originated around 1 Ma. These results are incongruent with younger molecular divergence estimates and suggest at least one of the following must be true: (i) European fossils and the [N-MH]LCA selectively retained primitive dental traits; (ii) molecular estimates of the divergence between Neanderthals and modern humans are underestimated; or (iii) phenotypic divergence and speciation between both species were decoupled such that phenotypic differentiation, at least in dental morphology, predated speciation.

Giant boid snake from the Palaeocene neotropics reveals hotter past equatorial temperatures.

The largest extant snakes live in the tropics of South America and southeast Asia where high temperatures facilitate the evolution of large body sizes among air-breathing animals whose body temperatures are dependant on ambient environmental temperatures (poikilothermy). Very little is known about ancient tropical terrestrial ecosystems, limiting our understanding of the evolution of giant snakes and their relationship to climate in the past. Here we describe a boid snake from the oldest known neotropical rainforest fauna from the Cerrejón Formation (58-60 Myr ago) in northeastern Colombia. We estimate a body length of 13 m and a mass of 1,135 kg, making it the largest known snake. The maximum size of poikilothermic animals at a given temperature is limited by metabolic rate, and a snake of this size would require a minimum mean annual temperature of 30-34 degrees C to survive. This estimate is consistent with hypotheses of hot Palaeocene neotropics with high concentrations of atmospheric CO(2) based on climate models. Comparison of palaeotemperature estimates from the equator to those from South American mid-latitudes indicates a relatively steep temperature gradient during the early Palaeogene greenhouse, similar to that of today. Depositional environments and faunal composition of the Cerrejón Formation indicate an anaconda-like ecology for the giant snake, and an earliest Cenozoic origin of neotropical vertebrate faunas.

Gene networks, occlusal clocks, and functional patches: new understanding of pattern and process in the evolution of the dentition.

Our understanding of the evolution of the dentition has been transformed by advances in the developmental biology, genetics, and functional morphology of teeth, as well as the methods available for studying tooth form and function. The hierarchical complexity of dental developmental genetics combined with dynamic effects of cells and tissues during development allow for substantial, rapid, and potentially non-linear evolutionary changes. Studies of selection on tooth function in the wild and evolutionary functional comparisons both suggest that tooth function and adaptation to diets are the most important factors guiding the evolution of teeth, yet selection against random changes that produce malocclusions (selectional drift) may be an equally important factor in groups with tribosphenic dentitions. These advances are critically reviewed here.

Challenges And Advances In Measuring Phenotypic Convergence.

Tests of phenotypic convergence can provide evidence of adaptive evolution, and the popularity of such studies has grown in recent years due to the development of novel, quantitative methods for identifying and measuring convergence. These methods include the commonly applied C1-C4 measures of Stayton (2015), which measure morphological distances between lineages, and Ornstein-Uhlenbeck (OU) model-fitting analyses, which test whether lineages converged on shared adaptive peaks. We test the performance of C-measures and other convergence measures under various evolutionary scenarios and reveal a critical issue with C-measures: they often misidentify divergent lineages as convergent. We address this issue by developing novel convergence measures- Ct1-Ct4-measures -that calculate distances between lineages at specific points in time, minimizing the possibility of misidentifying divergent taxa as convergent. Ct-measures are most appropriate when focal lineages are of the same or similar geologic ages (e.g., extant taxa), meaning that the lineages' evolutionary histories include considerable overlap in time. Beyond C-measures, we find that all convergence measures are influenced by the position of focal taxa in phenotypic space, with morphological outliers often statistically more likely to be measured as strongly convergent. Further, we mimic scenarios in which researchers assess convergence using OU models with a priori regime assignments (e.g., classifying taxa by ecological traits) and find that multiple-regime OU models with phenotypically divergent lineages assigned to a shared selective regime often outperform simpler models. This highlights that model support for these multiple-regime OU models should not be assumed to always reflect convergence among focal lineages of a shared regime. Our new Ct1-Ct4-measures provide researchers with an improved comparative tool, but we emphasize that all available convergence measures are imperfect, and researchers should recognize the limitations of these methods and use multiple lines of evidence to test convergence hypotheses.

Mammal disparity decreases during the Cretaceous angiosperm radiation.

Fossil discoveries over the past 30 years have radically transformed traditional views of Mesozoic mammal evolution. In addition, recent research provides a more detailed account of the Cretaceous diversification of flowering plants. Here, we examine patterns of morphological disparity and functional morphology associated with diet in early mammals. Two analyses were performed: (i) an examination of diversity based on functional dental type rather than higher-level taxonomy, and (ii) a morphometric analysis of jaws, which made use of modern analogues, to assess changes in mammalian morphological and dietary disparity. Results demonstrate a decline in diversity of molar types during the mid-Cretaceous as abundances of triconodonts, symmetrodonts, docodonts and eupantotherians diminished. Multituberculates experience a turnover in functional molar types during the mid-Cretaceous and a shift towards plant-dominated diets during the late Late Cretaceous. Although therians undergo a taxonomic expansion coinciding with the angiosperm radiation, they display small body sizes and a low level of morphological disparity, suggesting an evolutionary shift favouring small insectivores. It is concluded that during the mid-Cretaceous, the period of rapid angiosperm radiation, mammals experienced both a decrease in morphological disparity and a functional shift in dietary morphology that were probably related to changing ecosystems.

Updated imaging and phylogenetic comparative methods reassess relative temporal lobe size in anthropoids and modern humans.

OBJECTIVES: Two decades ago, Rilling and Seligman, hereafter abbreviated to RAS Study, suggested modern humans had relatively larger temporal lobes for brain size compared to other anthropoids. Despite many subsequent studies drawing conclusions about the evolutionary implications for the emergence of unique cerebral specializations in Homo sapiens, no re-assessment has occurred using updated methodologies. METHODS: We reassessed the association between right temporal lobe volume (TLV) and right hemisphere volume (HV) in the anthropoid brain. In a sample compiled de novo by us, T1-weighted in vivo Magnetic Resonance Imaging (MRI) scans of 11 extant anthropoid species were calculated by-voxel from the MRI and the raw data from RAS Study directly compared to our sample. Phylogenetic Generalized Least-Squares (PGLS) regression and trait-mapping using Blomberg's K (kappa) tested the correlation between HV and TLV accounting for anthropoid phylogeny, while bootstrapped PGLS regressions tested difference in slopes and intercepts between monkey and ape subsamples. RESULTS: PGLS regressions indicated statistically significant correlations (r2 < 0.99; p ≤ 0.0001) between TLV and HV with moderate influence from phylogeny (K ≤ 0.42). Bootstrapped PGLS regression did not show statistically significant differences in slopes between monkeys and apes but did for intercepts. In our sample, human TLV was not larger than expected for anthropoids. DISCUSSION: Updated imaging, increased sample size and advanced statistical analyses did not find statistically significant results that modern humans possessed a disproportionately large temporal lobe volume compared to the general anthropoid trend. This has important implications for human and non-human primate brain evolution.

Detecting Mismatch in Functional Narratives of Animal Morphology: a Test Case With Fossils.

A boom in technological advancements over the last two decades has driven a surge in both the diversity and power of analytical tools available to biomechanical and functional morphology research. However, in order to adequately investigate each of these dense datasets, one must often consider only one functional narrative at a time. There is more to each organism than any one of these form-function relationships. Joint performance landscapes determined by maximum likelihood are a valuable tool that can be used to synthesize our understanding of these multiple functional hypotheses to further explore an organism's ecology. We present an example framework for applying these tools to such a problem using the morphological transition of ammonoids from the Middle Triassic to the Early Jurassic. Across this time interval, morphospace occupation shifts from a broad occupation across Westermann Morphospace to a dense occupation of a region emphasizing an exposed umbilicus and modest frontal profile. The hydrodynamic capacities and limitations of the shell have seen intense scrutiny as a likely explanation of this transition. However, conflicting interpretations of hydrodynamic performance remain despite this scrutiny, with scant offerings of alternative explanations. Our analysis finds that hydrodynamic measures of performance do little to explain the shift in morphological occupation, highlighting a need for a more robust investigation of alternative functional hypotheses that are often intellectually set aside. With this we show a framework for consolidating the current understanding of the form-function relationships in an organism, and assess when they are insufficiently characterizing the dynamics those data are being used to explain. We aim to encourage the broader adoption of this framework and these ideas as a foundation to bring the field close to comprehensive synthesis and reconstruction of organisms.

Stops making sense: translational trade-offs and stop codon reassignment.

BACKGROUND: Efficient gene expression involves a trade-off between (i) premature termination of protein synthesis; and (ii) readthrough, where the ribosome fails to dissociate at the terminal stop. Sense codons that are similar in sequence to stop codons are more susceptible to nonsense mutation, and are also likely to be more susceptible to transcriptional or translational errors causing premature termination. We therefore expect this trade-off to be influenced by the number of stop codons in the genetic code. Although genetic codes are highly constrained, stop codon number appears to be their most volatile feature. RESULTS: In the human genome, codons readily mutable to stops are underrepresented in coding sequences. We construct a simple mathematical model based on the relative likelihoods of premature termination and readthrough. When readthrough occurs, the resultant protein has a tail of amino acid residues incorrectly added to the C-terminus. Our results depend strongly on the number of stop codons in the genetic code. When the code has more stop codons, premature termination is relatively more likely, particularly for longer genes. When the code has fewer stop codons, the length of the tail added by readthrough will, on average, be longer, and thus more deleterious. Comparative analysis of taxa with a range of stop codon numbers suggests that genomes whose code includes more stop codons have shorter coding sequences. CONCLUSIONS: We suggest that the differing trade-offs presented by alternative genetic codes may result in differences in genome structure. More speculatively, multiple stop codons may mitigate readthrough, counteracting the disadvantage of a higher rate of nonsense mutation. This could help explain the puzzling overrepresentation of stop codons in the canonical genetic code and most variants.

History matters: ecometrics and integrative climate change biology.

Climate change research is increasingly focusing on the dynamics among species, ecosystems and climates. Better data about the historical behaviours of these dynamics are urgently needed. Such data are already available from ecology, archaeology, palaeontology and geology, but their integration into climate change research is hampered by differences in their temporal and geographical scales. One productive way to unite data across scales is the study of functional morphological traits, which can form a common denominator for studying interactions between species and climate across taxa, across ecosystems, across space and through time-an approach we call 'ecometrics'. The sampling methods that have become established in palaeontology to standardize over different scales can be synthesized with tools from community ecology and climate change biology to improve our understanding of the dynamics among species, ecosystems, climates and earth systems over time. Developing these approaches into an integrative climate change biology will help enrich our understanding of the changes our modern world is undergoing.