Browsing by Author "McGlothlin, Joel W."

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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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    Adaptive radiation along a deeply conserved genetic line of least resistance in Anolis lizards
    McGlothlin, Joel W.; Kobiela, Megan E.; Wright, Helen V.; Mahler, Luke D.; Kolbe, Jason K.; Losos, Jonathan B.; Brodie, Edmund D. III (Wiley, 2018)
    On microevolutionary timescales, adaptive evolution depends upon both natural selection and the underlying genetic architecture of traits under selection, which may constrain evolutionary outcomes. Whether such genetic constraints shape phenotypic diversity over macroevolutionary timescales is more controversial, however. One key prediction is that genetic constraints should bias the early stages of species divergence along “genetic lines of least resistance” defined by the genetic (co)variance matrix, G. This bias is expected to erode over time as species means and G matrices diverge, allowing phenotypes to evolve away from the major axis of variation. We tested for evidence of this signal in West Indian Anolis lizards, an iconic example of adaptive radiation. We found that the major axis of morphological evolution was well aligned with a major axis of genetic variance shared by all species despite separation times of 20–40 million years, suggesting that divergence occurred along a conserved genetic line of least resistance. Further, this signal persisted even as G itself evolved, apparently because the largest evolutionary changes in G were themselves aligned with the line of genetic least resistance. Our results demonstrate that the signature of genetic constraint may persist over much longer timescales than previously appreciated, even in the presence of evolving genetic architecture. This pattern may have arisen either because pervasive constraints have biased the course of adaptive evolution or because the G matrix itself has been shaped by selection to conform to the adaptive landscape.
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    Assessing age, breeding stage, and mating activity as drivers of variation in the reproductive microbiome of female tree swallows
    Hernandez, Jessica; Hucul, Catherine; Reasor, Emily; Smith, Taryn; McGlothlin, Joel W.; Haak, David C.; Belden, Lisa K.; Moore, Ignacio T. (Wiley, 2021-07)
    Sexually transmitted microbes are hypothesized to influence the evolution of reproductive strategies. Though frequently discussed in this context, our understanding of the reproductive microbiome is quite nascent. Indeed, testing this hypothesis first re-quires establishing a baseline understanding of the temporal dynamics of the reproductive microbiome and of how individual variation in reproductive behavior and age influence the assembly and maintenance of the reproductive microbiome as a whole. Here, we ask how mating activity, breeding stage, and age influence the reproductive microbiome. We use observational and experimental approaches to explain variation in the cloacal microbiome of free- living, female tree swallows (Tachycineta bicolor). Using microsatellite- based parentage analyses, we determined the number of sires per brood (a proxy for female mating activity). We experimentally increased female sexual activity by administering exogenous 17ß-estradiol. Lastly, we used bacterial 16S rRNA amplicon sequencing to characterize the cloacal microbiome. Neither the number of sires per brood nor the increased sexual activity of females significantly influenced female cloacal microbiome richness or community structure. Female age, however, was positively correlated with cloacal microbiome richness and influenced overall community structure. A hypothesis to explain these patterns is that the effect of sexual activity and the number of mates on variation in the cloacal microbiome manifests over an individual's lifetime. Additionally, we found that cloacal microbiome alpha diversity (Shannon Index, Faith's phylogenetic distance) decreased and community structure shifted between breeding stages. This is one of few studies to document within-individual changes and age- related differences in the cloacal microbiome across successive breeding stages. More broadly, our results contribute to our understanding of the role that host life history and behavior play in shaping the cloacal microbiomes of wild birds.
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    Biology and conservation of the endangered Bahama Swallow (Tachycineta cyaneoviridis)
    Wilson, Maya (Virginia Tech, 2020-01-02)
    In order to prevent species extinctions, conservation strategies need to incorporate the identification and mitigation of the root causes of population decline with an assessment of vulnerability to genetic and stochastic factors affecting small populations. Species or populations with small ranges, such as those on islands, are particularly vulnerable to extinction, and deficient knowledge of these species often impedes conservation efforts. The Bahama Swallow (Tachycineta cyaneoviridis) is an endangered secondary cavity-nester that only breeds on three islands in the northern Bahamas: Abaco, Grand Bahama, and Andros. I investigated questions related to population size and distribution, genetic diversity and population structure, breeding biology, and ecological interactions of the swallow, with the goal of informing the conservation and management of the species. Using several population survey methods on Abaco, I found that swallow site occupancy and density is higher in southern Abaco, especially near roads and pine snags. Future research should prioritize identifying the causes of variable and low population densities in parts of the swallow's range. I used microsatellite markers and morphometrics to assess differences between populations on Abaco and Andros. We found a lack of genetic differentiation (G'ST = 0.03) between populations, but differences in morphology suggest that gene flow might be low enough to enable traits under selection to diverge. By locating and monitoring nests, I found that swallows rely on woodpecker-excavated cavities in pine snags and utility poles, and that swallows nesting in pine snags had higher fledging success (92%) than those nesting in utility poles (50-62%). Using a cavity nest-web approach, I assessed how swallows interact with cavity-nesting birds and resources on Abaco. Hairy Woodpeckers (Dryobates villosus) primarily excavated pine snags, while West Indian Woodpeckers (Melanerpes superciliaris) excavated utility poles in non-pine habitat. Only swallows and La Sagra's Flycatchers (Myiarchus sagrae) used nest sites in the pine forest. Swallows in non-pine habitat face competition for cavities with American Kestrels (Falco sparverius), and non-native House Sparrows (Passer domesticus) and European Starlings (Sturnus vulgaris). These results highlight the importance of pine forest and the Hairy Woodpecker for the persistence of the swallow.
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    The causes and consequences of variation in the cloacal microbiome of tree swallows (Tachycineta bicolor)
    Hernandez, Jessica (Virginia Tech, 2021-08-31)
    Animals are ecological landscapes that host communities of microbes often referred to as microbiomes. These microbes can be transferred between individuals when they come into contact, such as during mating. Microbes that reside in or on any aspect of a host that becomes exposed to the reproductive tract or gametes comprise the reproductive microbiome. These microbes within the reproductive microbiome are important to overall host biology because they can influence host reproductive function, and thus play a role in shaping host ecology, evolution, and fitness. Though previous work has revealed much about the impact of beneficial and pathogenic microbes within the reproductive tract, much is left to be learned from describing the dynamic nature of the reproductive microbiome, and ultimately, how it affects host fitness. For my dissertation, I asked questions regarding how and why reproductive microbiome diversity varies among individuals. For instance, does reproductive microbiome diversity vary with respect to the number of mates or mating activity? Does reproductive microbiome diversity vary with host age or breeding stage? Are there fitness consequences associated with differences in reproductive microbiome diversity? To explore these questions, I studied tree swallows (Tachycineta bicolor), a socially monogamous bird in which both females and males engage in extra-pair mating activity. I focused on the cloacal microbiome as it is the site of contact during mating, and thus where microbes can be sexually transferred between individuals. I found that social partners did not have more similar cloacal microbiome diversity compared to other individuals in the same population, and that cloacal microbiome diversity was similar between sexes (Chapter II). By combining an observational approach with a hormone implant manipulation, I found that neither the number of sires per brood nor the increased mating activity of females significantly influenced cloacal microbiome richness or community structure. However, female age and breeding stage did significantly correlate with cloacal microbiome richness and community structure (Chapter III). Based on these findings, I hypothesized that the effect of mating activity on variation in the cloacal microbiome may only be detectable over a female's lifetime, and not within a single breeding season. In addition, I found evidence for a relationship between lay date and cloacal microbiome structure, after controlling for age. And I found that older females lay earlier in the season compared to younger, first-time breeding females (Chapter IV). These results provide support for a relationship between lay date and the cloacal microbiome and highlight the importance of age to this relationship. Lastly, I discussed future steps that can be taken to extend the framework established by my dissertation research, and thereby gain further insight into the factors shaping the reproductive microbiome (Chapter V).
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    Effects of urbanization on the physiology, behavior, and fitness of a wild songbird
    Lane, Samuel Joseph (Virginia Tech, 2022-09-14)
    As urbanization spreads, understanding its impact on wildlife is increasingly urgent. By comparing the traits and fitness of individuals within the same species found in both urban and rural habitats (urban adapters), we can better understand the behavioral and physiological coping mechanisms wild birds employ in the face of rapid environmental change. For my dissertation, I investigated the physiological, behavioral, and fitness differences between urban and rural living song sparrows (Melospiza melodia) to explore how song sparrows are adjusting to urban environments. In my first chapter, I investigated urban birds' termination of the glucocorticoid stress response by looking at their ability to reduce circulating levels of glucocorticoid 'stress' hormones and the relative abundance of receptors that provide negative feedback in the hippocampus and hypothalamus. I found that urban males have a lower relative abundance of glucocorticoid receptors and the enzyme 11β-HSD2 in the hippocampus compered too rural, though we found no difference in negative feedback at the periphery, as both urban and rural song sparrows responded similarly to a challenge with synthetic glucocorticoid (dexamethasone). In chapter 2, I asked if increased aggression, which has been rigorously documented in urban males, is also expressed by females, and whether this aggressive signaling is constraining other reproductive behaviors such as maternal care. Indeed, female song sparrows, like males, expressed increased aggressive signaling compared to rural, suggesting urban habitats may favor a more aggressive phenotype. Finally, in Chapter 3, I investigated the consequences of increased male aggression on their social partners and offspring by measuring parental care and nestling outcomes across urban and rural habits. I was unable to establish a trade-off between parental care and aggression in either sex, suggesting this increased aggression is not constraining other reproductive behaviors. In fact, the more aggressive urban males visited the nest significantly more frequently, a trend also seen in urban females during the daylight hours, though the relationship was not significant over a 24-hour period. Additionally, urban birds had significantly higher reproductive metrics compared to rural, though they also had the added cost of increase brood parasitism by brown-headed cowbirds (Molothrus ater) compared to rural. Overall increased urban aggression was associated with higher reproductive success without any reduction in paternal care. Additionally, we found physiological differences in the glucocorticoid stress response system associated with the differences in habitat but whether theses differences represent mechanisms of acclimation or potential costs of living in urban habitats is not yet clear.
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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 Populus trichocarpa (Western Poplar)
    Bawa, Rajesh Kumar (Virginia Tech, 2017-08-15)
    Forest trees are an important pool of biodiversity at the gene, individual and an ecosystem level. This variation is a result of complex environmental interactions, as well as neutral and selective forces acting on populations. Patterns of standing genetic variation are the result of adaption to past and contemporary climate change, but also historical demographic events, and disentangling the role of these forces is a central problem in population genomics. The overall goal of this study is to characterize the relative effects of demography and selection in the genome of Populus trichocarpa, a riparian deciduous tree species of North America. Specifically, I used a variety of methods to summarize patterns of genetic diversity and population structure in P. trichocarpa, and to reconstruct its demographic history. I subsequently incorporated these demographic insights to guide the application of several methods to identify genome-wide targets of natural selection within and among rangewide populations adapted to heterogeneous selection regimes. Results of this study provide insights into the history of divergence and differentiation in P. trichocarpa populations and help us identify the functional genetic variants contributing to phenotypic divergence and fitness of the individuals in it.
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    Exploring the drivers and consequences of emerging infectious disease of wildlife
    Grimaudo, Alexander Thomas (Virginia Tech, 2024-04-22)
    Emerging infectious diseases of wildlife have threatened host populations of diverse taxa in recent history, which is largely attributable to anthropogenic global change. In three data chapters, this dissertation examines the drivers of individual- to population-level variation in how host populations respond to novel and emerging pathogens. Each chapter explores these processes in bat populations of North America, predominantly the Northeast and Midwest regions of the United States, impacted by the emerging fungal pathogen that causes white-nose syndrome, Pseudogymnoascus destructans. In Chapter 2, I disentangle the effects of adaptive host traits and environmental influences in driving host population stabilization of the little brown bat (Myotis lucifugus), finding that host-pathogen coexistence in this system is the product of their complex interaction. In Chapter 3, I characterize the range-wide variation in white-nose syndrome impacts on a federally endangered and poorly studied species, the Indiana bat (Myotis sodalis), as well as environmental and demographic determinants of its declines over epidemic time. In Chapter 4, I explore the role of individual variation in roosting microclimate selection of little brown bats in driving their infection severity, yielding important insights into the pathophysiology and environmental dependence of white-nose syndrome. Ultimately, this dissertation characterizes complex drivers of variation in host responses to emerging and invading pathogens, yielding insights essential to the successful mitigation of their impacts.
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    Exposure heterogeneity, host immunity and virulence evolution in a wild bird-bacterium system
    Leon, Ariel Elizabeth (Virginia Tech, 2019-06-25)
    Immunological heterogeneity is the norm in most free-living vertebrate populations, creating a diverse and challenging landscape for pathogens to replicate and transmit. This dissertation work sought to determine sources of immunological heterogeneity, as well as the consequences of this heterogeneity on pathogen fitness and evolution. A major source of heterogeneity in free-living host populations is the degree of exposure to a pathogen, as well as a host's history of exposure to a pathogen, which can create variation in standing immunity. We sought to determine the role of exposure heterogeneity on host susceptibility and immunity to secondary infection, and the influence of this heterogeneity on pathogen fitness and virulence evolution in a wild bird-bacterium system. We first determined that exposure level has a significant effect on host susceptibility to infection, severity of disease and infection, as well as immunity produced to secondary infection. Subsequently, we tested whether exposure history, and the immunity formed from this previous exposure, altered the within-host fitness advantage to virulent pathogens. We determined that previous low-level repeat exposure, which wild hosts likely encounter while foraging, produces a within-host environment which greatly favors more virulent pathogens. While within-host processes are vital for understanding and interpreting the evolutionary pressures on a pathogen, the ultimate metric of pathogen fitness is transmission. We therefore tested whether exposure history altered the transmission potential of a host and whether prior host exposure selected for more virulent pathogens. The transmission potential of a host significantly decreased with previous exposure, and high levels of previous exposure selected for more virulent pathogens. While we anticipated selection to be strongest at low-levels of exposure based on our previous results, we found here that high doses of prior exposure resulted in the strongest transmission advantage to virulence. This study also provided insight into the nuanced nature of transmission, which our results indicate is determined both by the degree of within-host pathogen replication as well as host disease severity. Together, our findings underscore the importance of exposure level and exposure history in natural populations in determining susceptibility, immunity and pathogen virulence evolution.
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    Gene Conversion Facilitates the Adaptive Evolution of Self-Resistance in Highly Toxic Newts
    Gendreau, Kerry L.; Hornsby, Angela D.; Hague, Michael T. J.; McGlothlin, Joel W. (Oxford Academic, 2021-10)
    Reconstructing the histories of complex adaptations and identifying the evolutionary mechanisms underlying their origins are two of the primary goals of evolutionary biology. Taricha newts, which contain high concentrations of the deadly toxin tetrodotoxin (TTX) as an antipredator defense, have evolved resistance to self-intoxication, which is a complex adaptation requiring changes in six paralogs of the voltage-gated sodium channel (Nav) gene family, the physiological target of TTX. Here, we reconstruct the origins of TTX self-resistance by sequencing the entire Nav gene family in newts and related salamanders. We show that moderate TTX resistance evolved early in the salamander lineage in three of the six Nav paralogs, preceding the proposed appearance of tetrodotoxic newts by ∼100 My. TTX-bearing newts possess additional unique substitutions across the entire Nav gene family that provide physiological TTX resistance. These substitutions coincide with signatures of positive selection and relaxed purifying selection, as well as gene conversion events, that together likely facilitated their evolution. We also identify a novel exon duplication within Nav1.4 encoding an expressed TTX-binding site. Two resistance-conferring changes within newts appear to have spread via nonallelic gene conversion: in one case, one codon was copied between paralogs, and in the second, multiple substitutions were homogenized between the duplicate exons of Nav1.4. Our results demonstrate that gene conversion can accelerate the coordinated evolution of gene families in response to a common selection pressure.
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    Hormonal pleiotropy structures genetic covariance
    Wittman, Tyler N.; Robinson, Christopher D.; McGlothlin, Joel W.; Cox, Robert M. (Wiley, 2021-06-13)
    Quantitative genetic theory proposes that phenotypic evolution is shaped by G, the matrix of genetic variances and covariances among traits. In species with separate sexes, the evolution of sexual dimorphism is also shaped by B, the matrix of between-sex genetic variances and covariances. Despite considerable focus on estimating these matrices, their underlying biological mechanisms are largely speculative. We experimentally tested the hypothesis that G and B are structured by hormonal pleiotropy, which occurs when one hormone influences multiple phenotypes. Using juvenile brown anole lizards (Anolis sagrei) bred in a paternal half-sibling design, we elevated the steroid hormone testosterone with slow-release implants while administering empty implants to siblings as a control. We quantified the effects of this manipulation on the genetic architecture of a suite of sexually dimorphic traits, including body size (males are larger than females) and the area, hue, saturation, and brightness of the dewlap (a colorful ornament that is larger in males than in females). Testosterone masculinized females by increasing body size and dewlap area, hue, and saturation, while reducing dewlap brightness. Control females and males differed significantly in G, but treatment of females with testosterone rendered G statistically indistinguishable from males. Whereas B was characterized by low between-sex genetic correlations when estimated between control females and males, these same correlations increased significantly when estimated between testosterone females and either control or testosterone males. The full G matrix (including B) for testosterone females and either control or testosterone males was significantly less permissive of sexually dimorphic evolution than was G estimated between control females and males, suggesting that natural sex differences in testosterone help decouple genetic variance between the sexes. Our results confirm that hormonal pleiotropy structures genetic covariance, implying that hormones play an important yet overlooked role in mediating evolutionary responses to selection.
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    Interacting phenotypes and the coevolutionary process: Interspecific indirect genetic effects alter coevolutionary dynamics
    De Lisle, Stephen P.; Bolnick, Daniel I.; Brodie, Edmund D., III; Moore, Allen J.; McGlothlin, Joel W. (Wiley, 2022-03)
    Coevolution occurs when species interact to influence one another's fitness, resulting in reciprocal evolutionary change. In many coevolving lineages, trait expression in one species is modified by the genotypes and phenotypes of the other, forming feedback loops reminiscent of models of intraspecific social evolution. Here, we adapt the theory of within-species social evolution, characterized by indirect genetic effects and social selection imposed by interacting individuals, to the case of interspecific interactions. In a trait-based model, we derive general expressions for multivariate evolutionary change in two species and the expected between-species covariance in evolutionary change when selection varies across space. We show that reciprocal interspecific indirect genetic effects can dominate the coevolutionary process and drive patterns of correlated evolution beyond what is expected from direct selection alone. In extreme cases, interspecific indirect genetic effects can lead to coevolution when selection does not covary between species or even when one species lacks genetic variance. Moreover, our model indicates that interspecific indirect genetic effects may interact in complex ways with cross-species selection to determine the course of coevolution. Importantly, our model makes empirically testable predictions for how different forms of reciprocal interactions contribute to the coevolutionary process.
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    Investigating the Patterns of Convergence in Pectoral Girdle Reduction During the Evolution of Limblessness in Lerista (Scincidae)
    Koeller, Krista Leslie Marie (Virginia Tech, 2020-12-23)
    Over 30 tetrapod groups have evolved a snake-like, elongate, limbless body plan. Studies of the patterns of limb reduction have revealed a close relationship between the reduction of the limbs and body elongation; however, the loss of the skeletal elements that support the limb, the pectoral girdle, has been less thoroughly examined. Here, I use computed tomography to generate three dimensional models of the pectoral girdles of an Australian skink genus, Lerista. This group contains pentadactyl species, fully limbless species and many species with intermediate morphologies. I employed a 3D geometric morphometric analysis to compare the shapes of these structures and revealed that the reduction of the pectoral girdle is correlated with the degree of loss in the limbs. The girdle in species with well developed limbs is longer and more narrow than the short, broad girdle of species with highly reduced or absent limbs, but the degree of reduction is only loosely correlated with the degree of reduction in the limbs. Certain events appear to occur concurrently such as the losses of the coracoid foramen and the humerus, but other events such as the loss of the epicoracoid are not consistently associated with any other event. The extent to which limb reduction is associated with the degree of pectoral girdle reduction and the morphology of the girdles appears to be closely associated with subclade, with individuals from closely related clades showing dramatically different degrees of girdle reduction despite similarities in the degree of limb loss. Despite these differences, the patterns in Lerista are generally more similar to each other than to those of other lizard groups, and more similar to those of other skinks than to those of other groups of lizards. Though some aspects of limb loss are common to all lizard groups that have evolved a serpentine body plan, this study shows that, even in closely related groups, this transition does not proceed in exactly the same way.
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    Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome
    Perry, Blair W.; Card, Daren C.; McGlothlin, Joel W.; Pasquesi, Giulia IM M.; Adams, Richard H.; Schield, Drew R.; Hales, Nicole R.; Corbin, Andrew B.; Demuth, Jeffery P.; Hoffmann, Federico G.; Vandewege, Michael W.; Schott, Ryan K.; Bhattacharyya, Nihar; Chang, Belinda SW W.; Casewell, Nicholas R.; Whiteley, Gareth; Reyes-Velasco, Jacobo; Mackessy, Stephen P.; Gamble, Tony; Storey, Kenneth B.; Biggar, Kyle K.; Passow, Courtney N.; Kuo, Chih-Horng; McGaugh, Suzanne E.; Bronikowski, Anne M.; de Koning, AP Jason P. J.; Edwards, Scott V.; Pfrender, Michael E.; Minx, Patrick; Brodie, Edmund D.; Brodie, Edmund D.; Warren, Wesley C.; Castoe, Todd A. (Oxford University Press, 2018-08-01)
    Colubridae represents themost phenotypically diverse and speciose family of snakes, yet nowell-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genomestructure that provide insight into the evolution of amniote genomes.Analyses of the garter snake andother squamate reptile genomes highlight shifts in repeat element abundance andexpansionwithin snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z andW sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionaryorigins ina rear-fanged colubridsnake, togetherwith newgenomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.
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    The Origins of Terpene Infochemicals in Insects: Identification and Evolutionary Analysis of Terpene Synthases in Diverse Lineages
    Rebholz, Zarley Alexander (Virginia Tech, 2024-09-10)
    Specialized metabolites have important roles as infochemicals in inter- and intraspecific interactions of insects. A particularly abundant class of specialized metabolites are terpenes, which are released by many members of taxonomically diverse insect lineages as pheromone and defense compounds. Despite the broad occurrence of terpenes in insects, knowledge of their biosynthesis remains limited compared to that in other forms of life. Terpenes are biosynthetically produced by the action of terpene synthase (TPS) enzymes. While insects lack TPS enzymes found in plants and microbes, there is growing evidence that insect TPS proteins have evolved independently from isoprenyl diphosphate synthase (IDS) enzymes in core terpene metabolism. To gain deeper insight into the transition from IDS to TPS function, I have explored the genomic and functional evolution of TPS enzymes in representatives of major insect lineages. First, I investigated evolutionary and functional relationships of TPS enzymes with roles in pheromone biosynthesis in pentatomids (stink bugs) including the invasive and economically critical pests Nezara viridula (Southern green stink bug) and Halyomorpha halys (brown marmorated stink bug). I also performed a comprehensive phylogenetic analysis of TPS genes in species across the broader order of piercing-sucking insects (Hemiptera), which provided evidence for an ancient emergence of TPS function in this group of insects. To gain a better understanding of core structural determinants of insect TPS evolution, we next defined distinct IDS catalytic motifs that are consistently substituted in enzymes with TPS function. These sequence characteristics were used to make predictions of TPS functionality in a large dataset of insect proteins. I determined the evolutionary dynamics of predicted and known TPS and IDS enzymes through extensive phylogenetic analysis to make top-level inferences about the distribution and evolution of TPS function in insects. Using this knowledge, I further explored functional transitions and subfunctionalization of TPS genes in the large order of beetles (Coleoptera), and more specifically, in species of the lady beetle family (Cocinellidae) including the globally invasive pest, Harmonia axyridis. Comparative genome analyses and IDS/TPS gene functional characterizations revealed gene duplication patterns and enzyme transitions that suggest TPS function evolved in part through processes of subfunctionalization and bifunctional enzymatic states. Additionally, this study provided the first experimental evidence for the mitochondrial localization of terpene metabolism in insects. Lastly, I identified putative TPS enzymes in the American cockroach, Periplaneta americana, and conducted an investigation into their catalytic activity. I found first evidence for TPS enzymatic activity in Blattodea as the most anciently diverging order of terpene-emitting insects and made inferences on the relationship of these enzymes to characterized IDS and TPS proteins in other insects. Our findings in the American cockroach point to the potential independent evolution of TPS function in blattodean cockroaches and termites in types of IDS ancestors. This work significantly advances our understanding of the evolution, functional diversity, and biochemical properties of TPS enzymes in insects, highlighting their recurring pattern of parallel evolution from IDS ancestors and its significance as a model for the emergence of novel specialized functions in core metabolic enzymes.
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    Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalis
    McGlothlin, Joel W.; Chuckalovcak, John P.; Janes, Daniel E.; Edwards, Scott V.; Feldman, Chris R.; Brodie, Edmund D.; Pfrender, Michael E.; Brodie, Edmund D. (Oxford University Press, 2014-08-18)
    Members of a gene family expressed in a single species often experience common selection pressures. Consequently, the molecular basis of complex adaptations may be expected to involve parallel evolutionary changes in multiple paralogs. Here, we use bacterial artificial chromosome library scans to investigate the evolution of the voltage-gated sodium channel (Nav) family in the garter snake Thamnophis sirtalis, a predator of highly toxic Taricha newts. Newts possess tetrodotoxin (TTX), which blocks Nav’s, arresting action potentials in nerves and muscle. Some Thamnophis populations have evolved resistance to extremely high levels of TTX. Previous work has identified amino acid sites in the skeletal muscle sodium channel Nav1.4 that confer resistance to TTX and vary across populations. We identify parallel evolution of TTX resistance in two additional Nav paralogs, Nav1.6 and 1.7, which are known to be expressed in the peripheral nervous system and should thus be exposed to ingested TTX. Each paralog contains at least one TTX-resistant substitution identical to a substitution previously identified in Nav1.4. These sites are fixed across populations, suggesting that the resistant peripheral nerves antedate resistant muscle. In contrast, three sodium channels expressed solely in the central nervous system (Nav1.1–1.3) showed no evidence of TTX resistance, consistent with protection from toxins by the blood–brain barrier. We also report the exon–intron structure of six Nav paralogs, the first such analysis for snake genes. Our results demonstrate that the molecular basis of adaptation may be both repeatable across members of a gene family and predictable based on functional considerations.
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    Phenotypic Responses to Invasion in the Brown Anole (Anolis sagrei)
    Fetters, Tamara Lynn (Virginia Tech, 2020-01-17)
    Invasive species often encounter climatic conditions that differ significantly from those of their native range. These environmental shifts may trigger phenotypic responses, resulting through some combination of adaptation and plasticity, that enable the invader to persist under novel thermal regimes. In this dissertation, I examine phenotypic changes in a tropical lizard that has successful invaded a cooler temperate climate, specifically examining traits that may promote survival and reproduction in their new range. First, I examined physiological traits, as I predicted greater cold tolerance would be necessary to survival in the invasive range. I found that invasive populations tolerated lower temperatures, exhibited greater maximum sprint speeds, and had higher metabolic rates than native populations. Next, I examined how life-history traits may change in the invasive range in order to facilitate reproduction under shorter breeding and growing seasons. I found that compared to native females, invasive females had shorter interlaying intervals and produced eggs that hatched more quickly. Once I quantified changes physiological and life-history traits that may have aided in successful establishment, I executed a common garden study to determine whether changes were the result of adaptation or plasticity. I found that differences in critical thermal minimum, metabolic rate, interlaying interval, and incubation period were maintained in lab-reared offspring, while measures of sprint speed converged. My results provide evidence that life history and physiology can evolve rapidly during invasion. These findings are useful to understanding contemporary evolution, and also provide valuable insight on how species respond to environmental shifts, both during invasions and as a result of climate change.
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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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    Potential Downstream Immunological Effects of Evolved Disease Tolerance in House Finches
    Rowley, Allison Annette (Virginia Tech, 2020-07-06)
    Emerging infectious diseases can exert strong selection on hosts to evolve resistance or tolerance to infection. However, it remains unknown whether the evolution of specific defense strategies against a novel pathogen influences host immune phenotypes more broadly, potentially affecting their ability to respond to other pathogens. In 1994 the bacterial pathogen, Mycoplasma gallisepticum (MG) jumped from poultry into house finches, causing severe conjunctivitis and reducing host survival. MG then spread across the continental United States, exerting strong selection on host populations and creating geographic variation in the degree of population co-evolutionary history with the pathogen. Prior work found that populations of house finches with longer histories of MG endemism have evolved tolerance and resistance to MG, and this evolution is associated with several immunological differences including reductions in pro-inflammatory immune responses. However, it remains unknown whether these immunological changes are limited to MG-specific defenses or whether broader immune responses differ between populations with distinct coevolutionary histories with MG. To examine possible effects of the evolution of host responses to MG, we used five immune assays to challenge house finches from four populations, ranging from no history of MG endemism to 20+ years of MG endemism. When challenged with phytohemagglutinin (PHA), populations differed significantly in the strength of wing web swelling, with populations with longer MG exposure (and thus the highest MG tolerance) on average exhibiting the weakest swelling response when mass differences were controlled for. However, detected population differences in wing web swelling were small, and population differences were absent for responses to four other immune assays that spanned components of the innate and adaptive immune system. Future work should examine whether the local inflammation that underlies swelling responses to PHA shares common immunological mechanisms with local inflammatory responses to MG, which may explain why populations with evolved tolerance to MG show slightly lower swelling responses in response to PHA. Overall, these results suggest that the evolution of MG tolerance may have minor downstream consequences for responses to certain antigens, with the potential to influence a host's ability to respond to novel pathogen challenges, but most components of the host immune system appear largely unaffected.