Browsing by Author "Uyeda, Josef C."

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    Adaptive evolution, sex-linkage, and gene conversion in the voltage-gated sodium channels of toxic newts and their snake predators
    Gendreau, Kerry (Virginia Tech, 2022-05-27)
    Understanding how genetic changes ultimately affect morphology and physiology is essential for understanding and predicting how organisms will adapt to environmental changes. Although most traits are complex and involve the interplay of many different genetic loci, some exceptions exist. These include the convergent evolution of tetrodotoxin resistance in snakes, which has a simple genetic basis and can be used as a model system to investigate the genetic basis of adaptive evolution. Tetrodotoxin is a potent neurotoxin used as a chemical defense by various animals, including toxic newts. Snakes have evolved resistance through mutations in voltage-gated sodium channels, the protein targets of tetrodotoxin, sparking an evolutionary arms race between predator and prey. In this dissertation, I describe how genomic rearrangements have led to sex-linkage of four of the voltage-gated sodium channel genes in snakes and compare allele frequencies across populations and sexes to make inferences about how sex linkage has influenced the evolution of resistance in garter snakes. By measuring gene expression in different snake tissues, I show that three of these sex-linked sodium channel genes are dosage compensated in embryos, adult muscle, and adult brain. In contrast, two channels show sexual dimorphism in their expression levels in the heart, which may indicate differences in dosage compensation among tissues. I then use comparative genomics to track the evolutionary history of tetrodotoxin resistance across all nine sodium channel genes in squamate reptiles and show how historical changes have paved the way for full-body resistance in certain snakes. Finally, I use targeted sequence capture to obtain the sodium channel sequences of salamanders and show evidence that tetrodotoxin self-resistance in toxic newts was likely accelerated through gene conversion between resistant and non-resistant sodium channel paralogs. Together, these results illustrate parallelism in evolutionary mechanisms and processes contributing to the appearance of an extreme and complex trait that arose independently in two distinct taxa separated by hundreds of millions of years.
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    Causal modeling refutes Hockett’s hypothesis that bite configuration affects human sound evolution
    Tarasov, Sergei; Uyeda, Josef C. (Virginia Tech, 2020-02-21)
    Blasi et al. (Research article, 15 March 2019) argue in support of Hockett’s hypothesis – that languages of hunter-gatherers are less likely to develop labiodental sounds than those of agricultural societies due to the former’s heavywear diet that favors edge-to-edge bite, thereby decreasing likelihood of labiodental articulation. We reanalyze the data in Blasi et al. and find little to no support in favor of the Hockett’s hypothesis. The negative association between labiodentals and hunter-gatherers instead appears to be an artifact of labiodental decline with increasing distance from Africa, which is a general trend of language phonemes.
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    Discovering Novel Biological Traits From Images Using Phylogeny-Guided Neural Networks
    Elhamod, Mohannad; Khurana, Mridul; Manogaran, Harish Babu; Uyeda, Josef C.; Balk, Meghan A.; Dahdul, Wasila; Bakış, Yasin; Bart, Henry L. Jr.; Mabee, Paula M.; Lapp, Hilmar; Balhoff, James P.; Charpentier, Caleb; Carlyn, David; Chao, Wei-Lun; Stewart, Charles V.; Rubenstein, Daniel I.; Berger-Wolf, Tanya; Karpatne, Anuj (ACM, 2023-08-06)
    Discovering evolutionary traits that are heritable across species on the tree of life (also referred to as a phylogenetic tree) is of great interest to biologists to understand how organisms diversify and evolve. However, the measurement of traits is often a subjective and labor-intensive process, making trait discovery a highly label-scarce problem. We present a novel approach for discovering evolutionary traits directly from images without relying on trait labels. Our proposed approach, Phylo-NN, encodes the image of an organism into a sequence of quantized feature vectors–or codes–where different segments of the sequence capture evolutionary signals at varying ancestry levels in the phylogeny. We demonstrate the effectiveness of our approach in producing biologically meaningful results in a number of downstream tasks including species image generation and species-to-species image translation, using fish species as a target example.
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    Evolution in biological radiations; insights from the Triassic archosaur radiation
    Hoffman, Devin Kane Fodor (Virginia Tech, 2022-06-29)
    Adaptive radiations, or evolutionary diversifications, are the evolutionary divergence of a single lineage into many different adaptive forms. They play a critical role in the history of life as groups of organisms speciate and fill new ecological roles over geologically rapid time intervals. There is currently no agreed upon operational unit, timeframe, or amount of divergence for organisms to be considered to have undergone an adaptive radiation. Additionally, the paucity of both comparative and fossil studies has limited the utility of the adaptive radiation in framing macroevolutionary questions, such as, is ecological and morphological diversification simultaneous? An ideal fossil clade to test this question is the Archosauriformes (crocodylians, birds, and their closest relatives). Archosauriforms radiated following the end-Permian mass extinction and their lineage diversification through the Early to Late Triassic is well documented in the literature. Prior to the end-Permian mass extinction, these reptiles were both species poor and ecologically limited, but by the Late Triassic they dominated terrestrial ecosystems in both species abundance and ecological breadth. However, continued environmental instability following the end-Permian extinction has led to the hypothesis that ecological expansion of archosauriforms lagged behind the diversification of lineages. The first chapter of my dissertation uses a Middle Triassic archosauriform tooth assemblage from Tanzania to reconstruct dietary specialization, estimated by morphological disparity of teeth. In addition to comparing tooth disparity of isolated and in situ teeth, this also provides a lens for comparing the timing of dietary specialization and species diversification. I found the archosauriforms to be faunivorous with little morphological disparity amongst the teeth. The second chapter uses an Early Triassic reptile tooth assemblage from South Africa to reconstruct the dietary specialization of archosauriforms early in their radiation to compare the amount of morphological disparity and lineage diversity. I use methods from Chapter 1 and integrate 3D morphometrics to better capture shape. I described several tooth morphotypes including six new to the locality. The morphological and dietary differences were minimal, indicating a greater species diversity than ecological diversity. The third chapter is a description of a new pseudosuchian archosaur taxon from the Middle Triassic of Tanzania. As species descriptions form the basic data unit of macroevolutionary analyses, this assists future studies of the archosauriform radiation. I recover this new taxon as the oldest known aetosaur. This species provides insights into the evolution of an armored carapace in crocodylian-line archosaurs and shows morphology related to armor evolved prior to the evolution of an herbivorous diet.
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    The evolution of convergence, growth, and diet under an adaptive landscape framework
    Wynd, Brenen Michael (Virginia Tech, 2022-03-23)
    Macroevolutionary patterns of adaptation are a product of natural selection acting on genetic and developmental variation within populations, the basis of microevolution. In microevolution, an adaptive landscape is used to visualize the relationship between phenotype and fitness, through a series of peaks and valleys. The adaptive landscape, as a concept suggests that there is some phenotypic optimum, or a combination of phenotypes, that result in a maximum fitness. This peak is not stable but is a reflection of interactions between the environment and the flora and fauna within. To expand the adaptive landscape to macroevolutionary scales is to assume that there is some optimum that a species or population is adapted to, and that numerous species can be compared to one another on the same landscape. The world of phylogenetic comparative methods uses the theory of the adaptive landscape in investigating the trajectory of trait change but is often limited to extant organisms. The fossil record often represents a major gap in the use of adaptive landscape theory, due in part to the incomplete nature of specimens or difficulties in untangling evolutionary relationships. Within this gap, the Triassic Period (252.2 – 201.5 MA) is sparsely represented, due to the often highly incomplete nature of Triassic fossils and our constantly evolving understanding of their phylogenetic relationships. However, the Triassic Period is bookended by mass extinctions, and is thus a useful case study to explore the utility of adaptive landscape theory for organisms in a time of rapid environmental change. My dissertation explores convergence and growth through an adaptive landscape framework, to reconstruct how species were evolving, or populations adapting, to a changing environment. The first chapter of my dissertation explores the evolution of a long snout in reptiles, with exploration of convergent evolution for both extant and extinct reptiles across the tree of life. The second chapter of my dissertation explores a statistical method to incorporate variation due to fossilization in estimating and quantifying growth curves. This second chapter was necessary to explore the third chapter of my dissertation, the ontogeny of a large-bodied mammal relative, Exaeretodon argentinus. With my third chapter, I quantify growth curves, compare them across other proto mammals closely related to Exaeretodon, and explore how diet may have changed over the lifetime of a single individual. These chapters focus on the adaptive landscape over different scales (population vs clade), and serve as a basis for future work in estimating dietary evolution.
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    Evolutionary Genomics of Dominant Bacterial and Archaeal Lineages in the Ocean
    Martinez Gutierrez, Carolina Alejandra (Virginia Tech, 2023-01-20)
    The ocean plays essential roles in Earth's biochemistry. Most of the nutrient transformations that fuel trophic webs in the ocean are mediated by microorganisms. The extent of phylogenetic and metabolic diversity of key culture and uncultured marine microbial clades started to be revealed due to progress in sequencing technologies, however we still lack a comprehensive understanding of the evolutionary processes that led to the microbial diversity we see in the ocean today. In this dissertation, I apply phylogenomic and comparative genomic methods to explore the evolutionary genomics of bacterial and archaeal clades that are relevant due to their abundance and biogeochemical activities in the ocean. In Chapter 1, I review relevant literature regarding the evolutionary genomics of marine bacteria and archaea, with emphasis on the origins of marine microbial diversity and the evolution of genome architecture. In Chapter 2, I use a comparative framework to get insights into the evolutionary forces driving genome streamlining in the Ca. Marinimicrobia, a clade widely distributed in the ocean. This project shows that differences in the environmental conditions found along the water column led to contrasting mechanisms of evolution and ultimately genome architectures. In Chapter 3, I assess the phylogenetic signal and congruence of marker genes commonly used for phylogenetic studies of bacteria and archaea and propose a pipeline and a set of genes that provide a robust phylogenetic signal for the reconstruction of multi-domain phylogenies. In Chapter 4, I apply a phylogeny-based statistical approach to evaluate how tightly genome size in bacteria and archaea is linked to evolutionary ii history, including marine clades. I present evidence suggesting that phylogenetic history and environmental complexity are strong drivers of genome size in prokaryotes. Lastly, in Chapter 5, I estimate the emergence time of marine bacterial and archaeal clades in the context of the Prokaryotic Tree of Life and demonstrate that the diversification of these groups is linked to the three main oxygenation periods occurring throughout Earth's history. I also identify the metabolic novelties that likely led to the colonization of marine realms. Here I present methodological frameworks in the fields of comparative genomics and phylogenomics to study the evolution of marine microbial diversity and show evidence suggesting that the main evolutionary processes leading to the extant diversity seen in the ocean today are intimately linked to geological and biological innovations occurring throughout Earth's history.
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    Exploring and Reconstructing Ancestral Anatomies using Ontology-Informed Approaches
    Tarasov, Sergei; Miko, Istvan; Yoder, Matthew; Uyeda, Josef C. (Pensoft, 2019-06-13)
    Ancestral character state reconstruction has been long used to gain insight into the evolution of individual traits in organisms. However, organismal anatomies (= entire phenotypes) are not merely ensembles of individual traits, rather they are complex systems where traits interact with each other due to anatomical dependencies (when one trait depends on the presence of another trait) and developmental constraints. Comparative phylogenetics has been largely lacking a method for reconstructing the evolution of entire organismal anatomies or organismal body regions. Herein, we present a new approach named PARAMO (Phylogenetic Ancestral Reconstruction of Anatomy by Mapping Ontologies, Tarasov and Uyeda 2019) that takes into account anatomical dependencies and uses stochastic maps (i.e., phylogenetic trees with an instance of mapped evolutionary history of characters, Huelsenbeck et al. 2003) along with anatomy ontologies to reconstruct organismal anatomies. Our approach treats the entire phenotype or its component body regions as single complex characters and allows exploring and comparing phenotypic evolution at different levels of anatomical hierarchy. These complex characters are constructed by ontology-informed amalgamation of elementary characters (i.e., those coded in character matrix) using stochastic maps. In our approach, characters are linked with the terms from an anatomy ontology, which allows viewing them not just as an ensemble of character state tokens but as entities that have their own biological meaning provided by the ontology. This ontologyinformed framework provides new opportunities for tracking phenotypic radiations and anatomical evolution of organisms, which we explore using a large dataset for the insect order Hymenoptera (sawflies, wasps, ants and bees).
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    Exploring the Soft Tissue of the Archosaurian Feeding System through Evolutionary and Developmental Temporal Space
    To, Khanh Hoang Thy (Virginia Tech, 2023-08-28)
    Tetrapods water-to-land transition in the Devonian was accompanied by an array of morphological modifications aiding in locomotion and food acquisition, which included diversification in teeth morphology. Different teeth morphology allowed tetrapods to take advantage of different ecological niches through food specialization. As useful as teeth are, we can see the repeated development of edentulous (=toothless) system throughout the fossil record, most frequently in Archosauria. Archosauria, represented today by living crocodylians and birds and includes extinct non-avian dinosaurs and pseudosuchians, first appeared in the early Mesozoic Era, during the Middle Triassic. Archosauria continue to diversify through the rest of the Mesozoic Era and during that time, we see a plethora of modifications made to the feeding apparatus in this group, such as dental batteries in hadrosaurids, bone crushing teeth in tyrannosaurids, or edentulous jaws covered in a rhamphotheca (=beak) in oviraptors. In the fossil record, morphological modifications can be seen in fossilized skeletal remains, but this is an incomplete picture of a living organism. The skeletal system of an organism is the housing and support, and it is powered by the muscles and ligaments and ultimately controlled by the nervous system. Without the soft tissues, we recognize that there are missing gaps in the anatomy, and modern organisms have been studied as analogs to fill these gaps. Traces of soft tissue are not completely undetectable in the fossil record. In exceptional preservation sites, materials such as keratinous integuments and gut materials have been found, but more commonly, we utilize osteological correlates such as muscle attachment scars that are derived from studying modern homologs to make inference about the presence of soft tissues. One advantage of using modern analogs to study soft tissue morphology is that we are able to incorporate how the targeted morphology grows through the observable developmental timescale. Ontogeny, or prenatal development and postnatal growth, has been utilized as an approach to understand how millions of years of natural selection affected the phenotypic expression in an organism. Through improvement of technology and laboratory techniques such as CT scanning and contrast-enhanced staining, in situ anatomical studies have revealed more information and details about the soft-tissue morphology in modern organisms to improve our interpretation of fossil organisms and address broader morphological macroevolution questions. This dissertation focuses on the construction and ontogenetic changes in the soft tissue (i.e., jaw muscles and keratinous sheath or rhamphotheca) and skeletal morphology of the avian edentulous feeding system and apply it to extinct edentulous feeding system across reptiles. My first chapter describes the ontogenetic changes in the musculoskeletal system of the jaws of emus (Dromaius novaehollandiae) to make inferences about potential influences of feeding function on the feeding apparatus during development. I combined microCT scanning, including contrast-stained CT scanning, and 3D geometric morphometric analyses to explore how the feeding apparatus changes through ontogeny and highlight intraspecific complexity within skeletally immature individuals. The second chapter explores the keratin layers making up the simple rhamphotheca of the chicken (Gallus gallus domesticus) and documents the varying mechanical properties within a single rhamphothecal sheath. This chapter establishes that biomechanical functions such as food and object manipulation affect the keratinous sheathing that covers the avian jaw bones by potentially selecting for specific regions of the rhamphotheca to be more mechanically resistant than others. In the third chapter, I review osteological correlates for rhamphotheca in modern edentulous taxa, birds and turtles, and in the extinct taxon, Trilophosaurus buettneri, a Late Triassic archosauromorph that was proposed to have both a beak and transversely-oriented teeth, to determine whether T. buettneri had a rhamphotheca and if so to what extent. This chapter reveals that one of the osteological correlates, foramina patterns, will benefit from future study that incorporates more turtle species and establishes that lack of wear on the oral/occlusal edge might be a valid osteological correlate to use for future fossil examination. These chapters showed a possible underlying influence of the feeding biomechanical function onto the anatomical construction and ontogeny in both the modern edentulous feeding system, providing an avenue for further exploration to address the repeated development of the edentulous feeding system.
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    Forelimb and Pectoral Anatomy of Arcticodactylus cromptonellus, an Early Pterosaur from the Late Triassic, and the Origins of Pterosaurs
    Fitch, Adam J. (Virginia Tech, 2024-01-16)
    Pterosaurs represent the earliest appearance of only three clades of flying vertebrates, the pioneers of aerial vertebrate ecospace, and the lineage to produce the largest known flying organisms. The origins of the pterosaurian flight apparatus have been difficult to ascertain, in part, due to incomplete or two-dimensional preservation of the earliest (Triassic—Jurassic) pterosaur remains. An exceptional early pterosaur specimen that is preserved in three dimensions, the holotype and only known specimen of Arcticodactylus cromptonellus (Fleming Fjord Formation, Greenland) may help address these problems. However, it has remained mostly encased within matrix to protect the delicate elements, obscuring external study. Here I present new synchrotron tomographic scan data of the forelimb (wing-forming) elements of Arcticodactylus cromptonellus. I find that the forelimb of Arcticodactylus is a structural intermediate between the forelimb of early archosaurs and derived pterosaurs. In light of this intermediacy, I reexamined the phylogeny of early Pterosauromorpha, completely reviewing forelimb characters with additional consideration given to other important anatomical regions for pterosauromorph phylogeny. I find that the contents of Lagerpetidae represent a grade of non-pterosaur pterosauromorphs and that the pterosauromorph Scleromochlus taylori is actually closely-related to crocodylomorphs. I recover Arcticodactylus as the earliest-diverging pterosaur, with the pterosaurs of the early Mesozoic (Triassic—Early Jurassic) forming a highly-nested, gradational relationship around a monophyletic Late Mesozoic pterosaur clade with very few multispecific groups exclusive of this latter clade. The sum of this work is an understanding of the current pterosaur fossil record as preserving the gradual assembly of the pterosaur bauplan in exquisite detail.
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    From genes to species: Characterizing spatial and temporal variation in frog and toad multidimensional biodiversity
    Moore, Chloe Ellen (Virginia Tech, 2023-05-15)
    Biodiversity is a complex concept encapsulating the variation that occurs within and among levels of biological organization. It is positively linked to ecosystem persistence, adaptability, and function. Biodiversity loss, driven by global change and human activities, is one of the most prominent threats to ecosystems. Characterizing the variation of and processes driving biodiversity is a critical step in understanding the causes, consequences, and magnitude of biodiversity loss. However, characterizing biodiversity comprehensively requires understanding multiple dimensions, or types, of diversity, such as genetic, taxonomic, phylogenetic, and life history diversity, that encompass both ecological and evolutionary processes varying across space and time. In this dissertation, I investigate spatial and temporal variation in frog and toad (order Anura) biodiversity to understand the effects of how diversity is measured on biodiversity characterization and the underlying processes driving biodiversity. In my first chapter, I examined the spatial and temporal variation of genetic diversity and other population genetic metrics to understand the effects of multi-year sampling on population genetic inference in an anuran metapopulation (Arizona treefrog, Hyla (Dryophytes) wrightorum). I found that a single sample year captures global, but not local, population genetic dynamics, as there is considerable temporal variation in genetic metrics within individual populations. In my second chapter, I developed a tool to improve the characterization of anuran life history diversity using species traits. Traits are the measurable attributes of species, and a suite of species traits is used to distinguish ecological strategies found among species. I collated trait data from 411 primary and secondary sources for 106 anuran species found in the United States to develop an anuran traits database for use in conservation, management, and research. In my third chapter, I investigated spatial variation within and among taxonomic, phylogenetic, and life history anuran diversity in the United States and examined the abiotic relationships behind observed patterns. To do this, I developed species distribution models at a 1 km2 resolution for the majority of the native US anurans. I identified relationships among diversity metrics for improved, comprehensive biodiversity characterization and potential ecological and evolutionary processes underlying biodiversity. Spatial variation in multidimensional relationships highlights regional needs for multiple metrics of diversity to comprehensively characterize biodiversity. This spatial variation is driven by temperature, elevation, and water availability, likely related to the biological limits for anurans. Collectively, these chapters highlight the considerable variation that exists within and among species of a broad and diverse biological. Furthermore, these chapters call attention to the importance of measuring multiple biodiversity dimensions for effective conservation in a rapidly changing world.
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    Host-pathogen interactions and conservation implications of snake fungal disease over broad geographical scales
    Blanvillain, Gaelle Jh (Virginia Tech, 2024-06-27)
    Emerging infectious diseases represent a threat to biodiversity, posing significant challenges to wildlife conservation globally. Infectious diseases can cause population declines, local extirpations and, in rare cases, complete species extinction. Among emerging pathogens, pathogenic fungi have been responsible for drastic declines in several high-profile vertebrate taxa, such as Batrachochytrium dendrobatidis causing chytridiomycosis in many species of amphibians worldwide. Recently, an emerging infectious disease, 'snake fungal disease' (SFD), caused by the fungal pathogen Ophidiomyces ophidiicola, is affecting the health of snake populations in North America by causing skin infections which can be fatal. Given the potential impact of this disease on snake biodiversity worldwide, compounded by the pressure of anthropogenic stressors that already jeopardize the viability of many snake populations, there is a clear need for ecological research in this understudied system. This dissertation is comprised of 4 data chapters focusing on the disease dynamics of snake fungal disease in Europe, and the factors resulting in differential infection. In chapter 2, I develop a large field-based data collection in 10 countries in Europe to investigate the presence of disease hotspots and the variation of disease prevalence across host species, and to examine the pathogen genotypes that are present on the landscape. I found isolated areas of disease hotspots, and models including an interactive effect of host species and which pathogen clade are present on the landscape were best at explaining disease prevalence. In chapter 3, I perform a virulence challenge assay using 120 corn snakes (Pantherophis guttatus) and 7 strains of O. ophidiicola (3 collected from Europe, 4 from the USA). This experiment reveals that pathogen genotypes associated with higher disease prevalence in Europe also have higher pathogen virulence, and that different strains from the USA show variation in virulence. These results also match both physiological host responses measured in the lab and landscape patterns of disease. In chapter 4, I explore two mitigation-driven snake translocation projects in Europe that were complicated due to O. ophidiicola outbreaks. One snake species, N. tessellata, appears highly susceptible to SFD, indicating that under stressful conditions, O. ophidiicola can cause mortality regardless of pathogen genotype, and that this snake species may be important in pathogen maintenance. Finally in chapter 5, I report the presence of a different fungal pathogen in Spain, Parannannizziopsis sp., never reported in wild snakes in Europe before. Broadly, my dissertation demonstrates coevolutionary relationships between hosts and pathogens and has important implications to snake conservation over large scales.
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    Including Distorted Specimens in Allometric Studies: Linear Mixed Models Account for Deformation
    Wynd, Brenen M.; Uyeda, Josef C.; Nesbitt, Sterling J. (Oxford Academic, 2021-05-18)
    Allometry—patterns of relative change in body parts—is a staple for examining how clades exhibit scaling patterns representative of evolutionary constraint on phenotype, or quantifying patterns of ontogenetic growth within a species. Reconstructing allometries from ontogenetic series is one of the few methods available to reconstruct growth in fossil specimens. However, many fossil specimens are deformed (twisted, flattened, and displaced bones) during fossilization, changing their original morphology in unpredictable and sometimes undecipherable ways. To mitigate against post burial changes, paleontologists typically remove clearly distorted measurements from analyses. However, this can potentially remove evidence of individual variation and limits the number of samples amenable to study, which can negatively impact allometric reconstructions. Ordinary least squares (OLS) regression and major axis regression are common methods for estimating allometry, but they assume constant levels of residual variation across specimens, which is unlikely to be true when including both distorted and undistorted specimens. Alternatively, a generalized linear mixed model (GLMM) can attribute additional variation in a model (e.g., fixed or random effects). We performed a simulation study based on an empirical analysis of the extinct cynodont, Exaeretodon argentinus, to test the efficacy of a GLMM on allometric data. We found that GLMMs estimate the allometry using a full dataset better than simply using only non-distorted data. We apply our approach on two empirical datasets, cranial measurements of actual specimens of E. argentinus (n = 16) and femoral measurements of the dinosaur Tawa hallae (n = 26). Taken together, our study suggests that a GLMM is better able to reconstruct patterns of allometry over an OLS in datasets comprised of extinct forms and should be standard protocol for anyone using distorted specimens.
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    Orb weaver capture thread biomechanics and evolution
    Kelly, Sean D. (Virginia Tech, 2020-07-07)
    Orb weavers intercept insects using non-hardening bioadhesive droplets, supported by two flagelliform fibers. Droplets contain an adhesive glycoprotein core and aqueous layer that confers hygroscopicity. The first study investigates the durability of these droplets to cycling, or repeatedly adhering, extending, and pulling off. Droplets of four species proved resilient, cycling 40 times. Cycling, coupled with droplet humidity responsiveness, qualifies them as smart materials. However, thread adhesion is complex, relying on an integrated performance of multiple droplets and the flagelliform fibers. As insects struggle, the flagelliform fibers bow and the droplets extend, forming a suspension bridge configuration whose biomechanics sum the adhesion of droplets and dissipate the energy of struggling insects. Given this performance, the second study predicts that the material properties of both thread components have evolved in a complementary way. Comparative phylogenetics of 14 study species revealed that their elastic moduli are correlated, with glycoproteins being six times more elastic than flagelliform fibers. Spider mass affects the amount of each material, but not their properties. Since glycoprotein performance changes with humidity, we hypothesized that orb weavers generate greater adhesion at their foraging humidity. After delimiting low and high humidity species groups (eight and six species, respectively), bridge force was determined as total contributing droplet adhesion at three humidities. Only three spiders generated greater adhesion outside of their foraging humidity. The distribution of force along a suspension bridge differed from a previously reported pattern. We also characterize the sheet configuration, which generates force similar to suspension bridges.
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    Phenoscape: Semantic analysis of organismal traits and genes yields insights in evolutionary biology
    Mabee, Paula M.; Dahdul, Wasila M.; Balhoff, James P.; Lapp, Hilmar; Manda, Prashanti; Uyeda, Josef C.; Vision, Todd; Westerfield, Monte (PeerJ, 2018-06-13)
    The study of how the observable features of organisms, i.e., their phenotypes, result from the complex interplay between genetics, development, and the environment, is central to much research in biology. The varied language used in the description of phenotypes, however, impedes the large scale and interdisciplinary analysis of phenotypes by computational methods. The Phenoscape project (www.phenoscape.org) has developed semantic annotation tools and a gene–phenotype knowledgebase, the Phenoscape KB, that uses machine reasoning to connect evolutionary phenotypes from the comparative literature to mutant phenotypes from model organisms. The semantically annotated data enables the linking of novel species phenotypes with candidate genes that may underlie them. Semantic annotation of evolutionary phenotypes further enables previously difficult or novel analyses of comparative anatomy and evolution. These include generating large, synthetic character matrices of presence/absence phenotypes based on inference, and searching for taxa and genes with similar variation profiles using semantic similarity. Phenoscape is further extending these tools to enable users to automatically generate synthetic supermatrices for diverse character types, and use the domain knowledge encoded in ontologies for evolutionary trait analysis. Curating the annotated phenotypes necessary for this research requires significant human curator effort, although semi-automated natural language processing tools promise to expedite the curation of free text. As semantic tools and methods are developed for the biodiversity sciences, new insights from the increasingly connected stores of interoperable phenotypic and genetic data are anticipated.
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    Phylogenetic Niche Modeling
    McHugh, Sean W. (Virginia Tech, 2021-09-01)
    Projecting environmental niche models through time is a common goal when studying species response to climatic change. Species distribution models (SDMs) are commonly used to estimate a species' niche from observed patterns of occurrence and environmental predictors. However, a species niche is also shaped by non-environmental factors--including biotic interactions and dispersal barrier—truncating SDM estimates. Though truncated SDMs may accurately predict present-day species niche, projections through time are often biased by environmental condition change. Modeling niche in a phylogenetic framework leverages a clade's shared evolutionary history to pull species estimates closer towards phylogenetic conserved values and farther away from species specific biases. We propose a new Bayesian model of phylogenetic niche implemented in R. Under our model, species SDM parameters are transformed into biologically interpretable continuous parameters of environmental niche optimum, breadth, and tolerance evolving under multivariate Brownian motion random walk. Through simulation analyses, we demonstrated model accuracy and precision that improved as phylogeny size increased. We also demonstrated our model on a clade of eastern United States Plethodontid salamanders by accurately estimating species niche, even when no occurrence data is present. Our model demonstrates a novel framework where niche changes can be studied forwards and backwards through time to understand ancestral ranges, patterns of environmental specialization, and niche in data deficient species.
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    Rise of present-day tetrapods in the paleotropics of Late Triassic equatorial Pangaea: new insights from microvertebrate data
    Kligman, Ben Thomas (Virginia Tech, 2023-05-09)
    The Triassic Period (~252–201.5 Ma) saw a transformative radiation and reorganization of continental tetrapod diversity following the end-Permian Extinction, including an assemblage of diverse forms that do not survive the end-Triassic (herein termed the 'endemic Triassic fauna', =ETF), as well as the earliest fossil representatives of all major modern tetrapod groups (herein termed the 'Living [Triassic to Recent] Fauna', =LTF; i.e. Salientia, Caudata, Gymnophiona, Mammaliaformes, Squamata, Rhynchocephalia, Testudinata, Crocodylomorpha, and Dinosauria). With few exceptions, only the LTF assemblage survives the end-Triassic Extinction (~201.5 Ma), highlighting the Late Triassic (~227–201.5 Ma) record as essential for understanding this pivotal transition and the evolutionary and ecological origins of post-Triassic non-marine tetrapod faunas, including those of present day. Micro-microvertebrate bonebeds are arguably the best proxy for tracking continental vertebrate biodiversity, however gaps in their Late Triassic record obscure patterns and drivers of evolutionary, ecological, and environmental change during the rise of LTF communities. In my dissertation, I use new data collected from Upper Triassic microvertebrate bonebeds from North America, and particularly the Thunderstorm Ridge site (PFV 456) in Petrified Forest National Park, Arizona, U.S.A, to fill gaps in the evolutionary record of specific groups (e.g., lissamphibians and lepidosaurs), as well as the vertebrate paleocommunity record of Triassic equatorial Pangaea. My first chapter describes and analyzes an assemblage of gymnophionomorph (stem caecilian) bones from PFV 456 which represent the oldest-known caecilian fossils globally. As the oldest caecilian fossils, they provide new support for the dissorophoid temnospondyl affinities of caecilians and other living amphibians, evidence of a step-wise acquisition of caecilian anatomies associated with fossoriality, and evidence of an ancient pattern of equatorial biogeographic restriction in caecilians from the Triassic to the present day. My second chapter describes and analyzes an assemblage of lepidosauromorphs from the Late Triassic of Equatorial Pangaea, providing new insights into the step-wise evolution tooth and jaw morphologies near the divergence of living lepidosaur clades (Squamata and Rhynchocephalia), and showing evidence for the Triassic acquisition in stem squamates and non-squamate lepidosaurs of dental features conserved in living squamates. The third chapter uses apomorphy-based identifications to describe the vertebrate diversity of the Thunderstorm Ridge site (PFV 456), providing evidence for the most species rich continental vertebrate community yet-known from the Triassic, with 55 vertebrate taxa. Nearly all LTF clades are present, predating similar assemblages from the early Jurassic by over 20 million years, and indicating that the assembly of the first LTF communities by at least 220 million years ago, long before the Triassic-Jurassic Extinction event (~201.5). The presence of this exceptional diversity may be linked to the climatic and environmental settings of equatorial Pangaea during the Triassic.
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    A timeline of bacterial and archaeal diversification in the ocean
    Martinez-Gutierrez, Carolina A.; Uyeda, Josef C.; Aylward, Frank O. (eLife Sciences, 2023-12)
    Microbial plankton play a central role in marine biogeochemical cycles, but the timing in which abundant lineages diversified into ocean environments remains unclear. Here, we reconstructed the timeline in which major clades of bacteria and archaea colonized the ocean using a high-resolution benchmarked phylogenetic tree that allows for simultaneous and direct comparison of the ages of multiple divergent lineages. Our findings show that the diversification of the most prevalent marine clades spans throughout a period of 2.2 Ga, with most clades colonizing the ocean during the last 800 million years. The oldest clades - SAR202, SAR324, Ca. Marinimicrobia, and Marine Group II - diversified around the time of the Great Oxidation Event, during which oxygen concentration increased but remained at microaerophilic levels throughout the Mid-Proterozoic, consistent with the prevalence of some clades within these groups in oxygen minimum zones today. We found the diversification of the prevalent heterotrophic marine clades SAR11, SAR116, SAR92, SAR86, and Roseobacter as well as the Marine Group I to occur near to the Neoproterozoic Oxygenation Event (0.8-0.4 Ga). The diversification of these clades is concomitant with an overall increase of oxygen and nutrients in the ocean at this time, as well as the diversification of eukaryotic algae, consistent with the previous hypothesis that the diversification of heterotrophic bacteria is linked to the emergence of large eukaryotic phytoplankton. The youngest clades correspond to the widespread phototrophic clades Prochlorococcus, Synechococcus, and Crocosphaera, whose diversification happened after the Phanerozoic Oxidation Event (0.45-0.4 Ga), in which oxygen concentrations had already reached their modern levels in the atmosphere and the ocean. Our work clarifies the timing at which abundant lineages of bacteria and archaea colonized the ocean, thereby providing key insights into the evolutionary history of lineages that comprise the majority of prokaryotic biomass in the modern ocean.
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    treedata.table: a wrapper for data.table that enables fast manipulation of large phylogenetic trees matched to data
    Román Palacios, Cristian; Wright, April; Uyeda, Josef C. (PeerJ, 2021-11-26)
    The number of terminals in phylogenetic trees has significantly increased over the last decade. This trend reflects recent advances in next-generation sequencing, accessibility of public data repositories, and the increased use of phylogenies in many fields. Despite R being central to the analysis of phylogenetic data, manipulation of phylogenetic comparative datasets remains slow, complex, and poorly reproducible. Here, we describe the first R package extending the functionality and syntax of data.table to explicitly deal with phylogenetic comparative datasets. treedata.table significantly increases speed and reproducibility during the data manipulation steps involved in the phylogenetic comparative workflow in R. The latest release of treedata.table is currently available through CRAN (https://cran.r-project.org/web/packages/treedata.table/). Additional documentation can be accessed through rOpenSci (https://ropensci.github.io/treedata.table/).