Browsing by Subject "Evolution & development"

Studies of skeletal variation form the basis of our understanding of our species’ history and diversity. This most commonly takes the form of comparative, between- species studies aimed at reconstructing phylogenetic relationships. However, studies of within-species variation can provide insights into relatedness at smaller scales, which can shed light on important microevolutionary processes and be used to identify closely related individuals in the absence of DNA. This dissertation assesses the relationship between genetic and skeletal variation within groups of related and unrelated Homo sapiens and Pan troglodytes, with the aim of better understanding the population sampled by the seemingly homogenous Homo naledi assemblage from the Dinaledi Chamber in Rising Star Cave, South Africa. The hypotheses tested were: 1) closely related individuals exhibit less skeletal variation compared to unrelated individuals, and 2) the Dinaledi assemblage exhibits less morphological variation than H. sapiens and P. troglodytes at the species level, more closely resembling a single population.

Skeletal variation within a subset of H. sapiens from the crypt of Christ Church in Spitalfields, London (17-19th centuries A.D) with documented genealogies and the Gombe population of P. t. schweinfurthii was compared to species-wide baselines and the H. naledi assemblage. The data consisted of 3D models of 556 postcranial elements (first metacarpal (Mc1), proximal femur, talus, calcaneus, and navicular) from 187 individuals that were generated from surface scanners or downloaded from MorphoSource.

This dissertation employed a relatively new 3D geometric morphometric workflow that captures the entire shape of an element through the use of an automated landmarking program and feature-aware registration process. Two hundred pseudolandmarks were automatically and optimally placed on each element. Following alignment, multiple univariate and multivariate statistical analyses were used to quantify shape variation within and between the three species, including distributions of Euclidean distances, Procrustes distances to the mean shapes, Principal Components Analyses (PCA), Between-Group PCA, and Discriminant Function Analyses. The coefficient of relationship was used to represent genetic distance between known genetic relatives within modern humans.

The results of the within-species analyses of skeletal variation support Hypothesis 1 in both modern humans and chimpanzees, though the signal of relatedness is differentially expressed within and across elements. In modern humans, the calcaneus can be used to distinguish known close relatives from distantly related and unrelated individuals. The navicular and femur were also found to be relatively good indicators of relatedness. Within chimpanzees, the talus is the most effective at distinguishing the Gombe population from the species-wide chimpanzee sample, followed by the calcaneus and femur. Within H. naledi, the talus varied the least while the navicular varied the most, though the high levels of variation found in the navicular and Mc1 are likely due to the state of preservation of these elements. The results of the interspecies analyses are more ambiguous. When considering the best preserved elements, the H. naledi talus varies the least within the three species, while the femur varies more than those of either H. sapiens or P. troglodytes at the species level. Hypothesis 2 is thus supported for the talus while rejected in the femur, suggesting that it cannot be rejected as a whole and that the patterns of homogeneity previously observed within H. naledi are more nuanced than previously recognized.

For primates, and other arboreal mammals, adopting suspensory locomotion represents one of the strategies an animal can use to prevent toppling off a thin support during arboreal movement and foraging. While numerous studies have reported the incidence of suspensory locomotion in a broad phylogenetic sample of mammals, little research has explored what mechanical transitions must occur in order for an animal to successfully adopt suspensory locomotion. Additionally, many primate species are capable of adopting a highly specialized form of suspensory locomotion referred to as arm-swinging, but few scenarios have been posited to explain how arm-swinging initially evolved. This study takes a comparative experimental approach to explore the mechanics of below branch quadrupedal locomotion in primates and other mammals to determine whether above and below branch quadrupedal locomotion represent neuromuscular mirrors of each other, and whether the patterns below branch quadrupedal locomotion are similar across taxa. Also, this study explores whether the nature of the flexible coupling between the forelimb and hindlimb observed in primates is a uniquely primate feature, and investigates the possibility that this mechanism could be responsible for the evolution of arm-swinging.

To address these research goals, kinetic, kinematic, and spatiotemporal gait variables were collected from five species of primate (Cebus capucinus, Daubentonia madagascariensis, Lemur catta, Propithecus coquereli, and Varecia variegata) walking quadrupedally above and below branches. Data from these primate species were compared to data collected from three species of non-primate mammals (Choloepus didactylus, Pteropus vampyrus, and Desmodus rotundus) and to three species of arm-swinging primate (Hylobates moloch, Ateles fusciceps, and Pygathrix nemaeus) to determine how varying forms of suspensory locomotion relate to each other and across taxa.

From the data collected in this study it is evident the specialized gait characteristics present during above branch quadrupedal locomotion in primates are not observed when walking below branches. Instead, gait mechanics closely replicate the characteristic walking patterns of non-primate mammals, with the exception that primates demonstrate an altered limb loading pattern during below branch quadrupedal locomotion, in which the forelimb becomes the primary propulsive and weight-bearing limb; a pattern similar to what is observed during arm-swinging. It is likely that below branch quadrupedal locomotion represents a “mechanical release” from the challenges of moving on top of thin arboreal supports. Additionally, it is possible, that arm-swinging could have evolved from an anatomically-generalized arboreal primate that began to forage and locomote below branches. During these suspensory bouts, weight would have been shifted away from the hindlimbs towards forelimbs, and as the frequency of these boats increased the reliance of the forelimb as the sole form of weight support would have also increased. This form of functional decoupling may have released the hindlimbs from their weight-bearing role during suspensory locomotion, and eventually arm-swinging would have replaced below branch quadrupedal locomotion as the primary mode of suspensory locomotion observed in some primate species. This study provides the first experimental evidence supporting the hypothetical link between below branch quadrupedal locomotion and arm-swinging in primates.

One of the most important questions in evolutionary biology is how new genes and new functions arise and evolve. Among the theories addressing this question, gene duplication is one of the most popular. Previous study has shown that two threonine deaminase (TD) gene copies exist in Solanum lycopersicum, and these two copies have very different functions and low sequence similarities. The primary objective of this study was to widen our understanding of this gene duplication and the subsequent evolutionary processes affecting the duplicate copies by first collecting additional TD sequences from related species, building a gene tree, and inferring the point of gene duplication. The evolutionary processes acting on this gene were then analyzed using the program PAML. Results indicate that 1) The TD duplication probably occurred in before the split of the Solanoideae from the Nicotianoidea; and 2) there is strong evidence for positive selection on one of the TD copies after gene duplication, while for the other TD copy, only weak evidence for positive selection was found; and 3) adaptive improvement of the copy with new function probably spanned a period of at least 25 million years.

Sex determination is a critical biological process for all sexually reproducing animals. Despite its significance, evolution has provided a vast array of mechanisms by which sexual phenotype is determined and elaborated even within amniote vertebrates. The most prevalent systems of sex determination in this clade are genetic and temperature dependent sex determination. These two systems are sometimes consistent within large groups of species, such as the mammals who nearly ubiquitously utilize XY genetic sex determination, or they can be much more mixed as in reptiles that use genetic or temperature dependent systems and even both simultaneously. The turtles are a particularly diverse group in the way they determine sex with multiple different genetic and temperature based systems having been described. We investigated the nature of the temperature based sex determination system in Trachemys scripta elegans to ascertain whether it behaved as a purely temperature based system or if some other global source of sex determining information might be apparent within thermal regions insufficient to fully induce male or female development. These experiments found that sex determination in this species is much more complex and early acting than previously thought and that each gonad within an individual has the same sexual fate established enough that it can persist even without further communication between. We established a best practice for the assembly and annotation of de novo whole transcriptomes from T. scripta RNA-seq and utilized the technique to quantify the gene regulatory events that occur across the thermal sensitive period.

Evidence is entirely lacking on the resolution of TSD when eggs are incubated at the pivitol temperature in which equal numbers or males and females are produces. We have produced a timecourse data set that allowed for the elucidation of the gene expression events that occur at both the MPT and FPT over the course of the thermal sensitive period. Our data suggests that early establishment of a male or female fate is possible when temperature is sufficiently strong enough as at MPT and FPT. We see a strong pattern of mutually antagonistic gene expression patterns emerging early and expanding over time through the end of the period of gonad plasticity. In addition, we have identified a strong pattern of differential expression in the early embryo at stages prior to the formation of the gonad. Even without the known systemic signaling attributed to sex hormones emanating from the gonad, the early embryo has a clear male and female gene expression pattern. We discuss how this early potential masculinization or feminization of the embryo may indicate that the influence of temperature may extend beyond the determination of gonadal sex or even metabolic adjustments and how this challenges the well-defined paradigm in which gonadal sex determines peripheral sexual characteristics.

Humans universally demonstrate intrinsically motivated prosocial behavior towards kin, non-kin ingroup members, and strangers. However, humans struggle to extend the same prosocial behavior to more abstract concepts like future-others and non-human species. The Adaptive Motivation Hypothesis posits that humans evolved intrinsic motivations to act prosocially towards more tangible social partners like those within an individual’s ingroup, but prosocial behavior towards more distant and abstract partners is constrained by ecological certainty. Prosocial behavior towards these more abstract concepts is more variable and more likely motivated by extrinsic reward. This dissertation aims to examine the development of motivations for prosocial behavior towards these more abstract concepts. My studies rely on common goods games as a proxy for examining behavior towards abstract recipients of prosocial behavior. Common goods are any resource like forests or fisheries that are non-excludable to a population, but rivalrous. In-demand common goods require cooperation of humans to ensure sustainable use in order to avoid depletion. Chapter One examined how children in three populations that differed in ecological certainty behaved in a common goods game where they were asked to contribute portions of their personal endowment to the maintenance of a forest. Participants were either provided a high extrinsic motivation, a low extrinsic motivation, or no extrinsic motivation for contributing to the maintenance of the common good. Results show that overall, children of all ages were more motivated to contribute to abstract recipients when extrinsic motivation is high. However, noticeable variation in behavior between populations was driven by ecological and cultural differences. Chapter Two examined whether aggregated extrinsic rewards increased contributions to common goods in a sample of children aged six to fourteen. Results suggest that both information about personal loss and delay in an acquiring resource together dramatically increase children’s contributions to common goods within both experimental and real-world contexts. Chapter Three explores whether making a typically abstract social partner more tangible increases an individual’s prosocial behavior towards said partner. Results for Chapter Three, conducted with a population in the Democratic Republic of the Congo, find that increasingly the tangibility of an abstract population marginally increases prosocial behavior in children but not in adults. Together, the results of these studies have implications improved understanding of the development of prosocial motivations in school age children, as well as applications to understanding motivations for socially conscious behavior in the face of environmental and conservation dilemmas.

Increased attention has recently been placed on understanding the natural variation of the malaria parasite Plasmodium vivax across the globe, as in 2020 alone, P. vivax caused an estimated 4.5 million malaria cases and lead to over 600,000 deaths around the world. P. vivax infections in central Africa have been of particular interest, as humans in Sub-Saharan Africa frequently possess a P. vivax resistance allele known as the Duffy-negative phenotype that is believed to prevent infection in these individuals. However, new reports of asymptomatic and symptomatic infections in Duffy-negative individuals in Africa raise the possibility that P. vivax is evolving to evade host resistance.Whole genome sequencing has become more common as a means of understanding the population diversity of P. vivax. However, there is still a scarcity of information about P. vivax in central Africa. In this dissertation, I analyze whole genome sequencing data from a new P. vivax sample collected from the Democratic Republic of the Congo in central Africa. By studying P. vivax from central Africa, we can begin to understand the evolutionary history of the pathogen in this part of the world as it relates to the global context of this pathogen. I also investigate the relationship of P. vivax in the DRC with a potential animal reservoir of a closely related species, P. vivax-like, in non-human primates in this region. Due to the scarcity of P. vivax samples in central Africa, I also investigated methods with which to best make use of whole genome sequencing data, particularly in generating phylogenetic trees. While many studies of P. vivax genetic diversity employ whole genome variation data in order to study evolutionary relationships of P. vivax populations, in this dissertation I make use of the P. vivax apicoplast, a non-photosynthetic plastid organelle genome. The apicoplast genome is five times longer than the mitochondrial genome and does not undergo recombination, making it a valuable locus for studying P. vivax evolutionary history using phylogenetic trees.

Admixture occurs when previously isolated populations come together to form a new population with genetic ancestry from those sources. Admixture is ubiquitous across the tree of life, including humans, and is often associated with migration and exposure to new environments and selective pressures. Admixed populations provide a unique opportunity to study adaptation on short timescales by introducing beneficial alleles at high frequency. However, admixed populations are often excluded from genomic studies due to lack of applicable methodology. Instead of relying on classical methods confounded by the process of admixture itself, we can detect changes in patterns of genetics ancestry that are informative about selection in admixed populations and at the short timescales often relevant for post-admixture selection. However, we lack theoretical expectations and methods to detect and characterize ancestry-based genomic signals indicative of post-admixture selection and adaptation. Common ancestry outlier approaches discard information about the surrounding genomic context and are prone to false positives due to drift and demography. Here, I present three studies which leverage patterns of genetic ancestry to investigate the evolutionary history of admixed populations. First, I develop a suite of ancestry-based summary statistics and computational methods to detect post-admixture adaptation, and demonstrate their application in a case study of human adaptation to malaria. In particular, these summary statistics incorporate patterns of ancestry beyond the site under selection, such as the length of contiguous ancestry tracts surrounding the locus, and are informative about the strength and timing of selection in admixed populations. I observe one of the strongest signals of recent selection in humans at the malaria protective Duffy-null allele, and show that this mode of strong single-locus selection over 20 generations has impacted genome-wide patterns of ancestry. Next, I move beyond summary statistics to develop a deep learning strategy for localizing regions of the genome under selection. This method takes images of chromosomes painted by ancestry as input to avoid the loss of information and bias that can occur when relying on user-defined summary statistics. I demonstrate this approach on simulated admixture scenarios and find that the method successfully localizes variants under selection 95% percent of the time, outperforms the common ancestry outlier approach, and is robust to demographic misspecification. Lastly, I present the first Illyrian genome sequences available from the Iron Age in a study of the ancestry and genetic relationships of five neonates buried in Korčula, Croatia. I find genetic support for classifying these individuals as Illyrian, and show that patterns of ancestry and genetic variation are consistent with their geographic location between Italy and the mainland Balkans. In the combined work presented here, I advance our ability to study the evolutionary history of admixed populations, which has implications for our understanding of phenotypic variation, disease risk, and conservation genetics across many study systems. Further, these methods tailored to the mosaic ancestry of admixed populations is a step towards expanding the diversity of populations, especially humans, who benefit from discoveries and advancement in genomic research.

A general goal of biology is to understand how two or more sets of traits in an organism are related - for example, disease state and genetics, physiology and behavior, or phenotypic variation and gene function. Many of the early advancements in statistical analysis dealt with relating measured traits when one could be represented as a single number. However, many traits are inherently multi-dimensional, and technologies are advancing for rapidly measuring many types of such highly complex traits. Making efficient use of these new, larger datasets requires new statistical models for to biological inference. In this thesis, I develop a method for relating two very different types of traits in sea urchin larvae: morphological shape, and developmental gene expression. In particular, I develop an approach for regression modeling using shape as a response variable. I use this method to address the question of whether variation in the expression of regulatory genes during development predicts later morphological variation in the larvae. I propose a hierarchical random effects factor regression model with shape as a response variable for relating morphology and gene expression when the individuals in each dataset are related, but not identical. I fit an approximation to the general model by breaking it into three discrete steps. I find that gene expression can explain ~25% of mean symmetric form variation among cultures of related larvae, and identify several groups of related genes that are correlated with aspects of morphological variation.

This thesis concerns the use of protein structure to improve phylogenetic inference. There has been growing interest in phylogenetics as the number of available DNA and protein sequences continues to grow rapidly and demand from other scientific fields increases. It is now well understood that phylogenies should be inferred jointly with alignment through use of stochastic evolutionary models. It has not been possible, however, to incorporate protein structure in this framework. Protein structure is more strongly conserved than sequence over long distances, so an important source of information, particularly for alignment, has been left out of analyses.

I present a stochastic process model for the joint evolution of protein primary and tertiary structure, suitable for use in alignment and estimation of phylogeny. Indels arise from a classic Links model and mutations follow a standard substitution matrix, while backbone atoms diffuse in three-dimensional space according to an Ornstein-Uhlenbeck process. The model allows for simultaneous estimation of evolutionary distances, indel rates, structural drift rates, and alignments, while fully accounting for uncertainty. The inclusion of structural information enables pairwise evolutionary distance estimation on time scales not previously attainable with sequence evolution models. Ideally inference should not be performed in a pairwise fashion between proteins, but in a fully Bayesian setting simultaneously estimating the phylogenetic tree, alignment, and model parameters. I extend the initial pairwise model to this framework and explore model variants which improve agreement between sequence and structure information. The model also allows for estimation of heterogeneous rates of structural evolution throughout the tree, identifying groups of proteins structurally evolving at different speeds. In order to explore the posterior over topologies by Markov chain Monte Carlo sampling, I also introduce novel topology + alignment proposals which greatly improve mixing of the underlying Markov chain. I show that the inclusion of structural information reduces both alignment and topology uncertainty. The software is available as plugin to the package StatAlign.

Finally, I also examine limits on statistical inference of phylogeny through sequence information models. These limits arise due to the `cutoff phenomenon,' a term from probability which describes processes which remain far from their equilibrium distribution for some period of time before swiftly transitioning to stationarity. Evolutionary sequence models all exhibit a cutoff; I show how to find the cutoff for specific models and sequences and relate the cutoff explicitly to increased uncertainty in inference of evolutionary distances. I give theoretical results for symmetric models, and demonstrate with simulations that these results apply to more realistic and widespread models as well. This analysis also highlights several drawbacks to common default priors for phylogenetic analysis, I and suggest a more useful class of priors.

The evolution of reproductive strategies involves a complex calculus of costs and benefits to both parents and offspring. Many marine animals produce embryos packaged in tough egg capsules or gelatinous egg masses attached to benthic surfaces. While these egg structures can protect against environmental stresses, the packaging is energetically costly for parents to produce. In this series of studies, I examined a variety of ecological factors affecting the evolution of benthic development as a life history strategy. I used marine gastropods as my model system because they are incredibly diverse and abundant worldwide, and they exhibit a variety of reproductive and developmental strategies.

The first study examines predation on benthic egg masses. I investigated: 1) behavioral mechanisms of predation when embryos are targeted (rather than the whole egg mass); 2) the specific role of gelatinous matrix in predation. I hypothesized that gelatinous matrix does not facilitate predation. One study system was the sea slug Olea hansineensis, an obligate egg mass predator, feeding on the sea slug Haminoea vesicula. Olea fed intensely and efficiently on individual Haminoea embryos inside egg masses but showed no response to live embryos removed from gel, suggesting that gelatinous matrix enables predation. This may be due to mechanical support of the feeding predator by the matrix. However, Haminoea egg masses outnumber Olea by two orders of magnitude in the field, and each egg mass can contain many tens of thousands of embryos, so predation pressure on individuals is likely not strong. The second system involved the snail Nassarius vibex, a non-obligate egg mass predator, feeding on the polychaete worm Clymenella mucosa. Gel neither inhibits nor promotes embryo predation for Nassarius, but because it cannot target individual embryos inside an egg mass, its feeding is slow and inefficient, and feeding rates in the field are quite low. However, snails that compete with Nassarius for scavenged food have not been seen to eat egg masses in the field, leaving Nassarius free to exploit the resource. Overall, egg mass predation in these two systems likely benefits the predators much more than it negatively affects the prey. Thus, selection for environmentally protective aspects of egg mass production may be much stronger than selection for defense against predation.

In the second study, I examined desiccation resistance in intertidal egg masses made by Haminoea vesicula, which preferentially attaches its flat, ribbon-shaped egg masses to submerged substrata. Egg masses occasionally detach and become stranded on exposed sand at low tide. Unlike adults, the encased embryos cannot avoid desiccation by selectively moving about the habitat, and the egg mass shape has high surface-area-to-volume ratio that should make it prone to drying out. Thus, I hypothesized that the embryos would not survive stranding. I tested this by deploying individual egg masses of two age classes on exposed sand bars for the duration of low tide. After rehydration, embryos midway through development showed higher rates of survival than newly-laid embryos, though for both stages survival rates over 25% were frequently observed. Laboratory desiccation trials showed that >75% survival is possible in an egg mass that has lost 65% of its water weight, and some survival (<25%) was observed even after 83% water weight lost. Although many surviving embryos in both experiments showed damage, these data demonstrate that egg mass stranding is not necessarily fatal to embryos. They may be able to survive a far greater range of conditions than they normally encounter, compensating for their lack of ability to move. Also, desiccation tolerance of embryos may reduce pressure on parents to find optimal laying substrata.

The third study takes a big-picture approach to investigating the evolution of different developmental strategies in cone snails, the largest genus of marine invertebrates. Cone snail species hatch out of their capsules as either swimming larvae or non-dispersing forms, and their developmental mode has direct consequences for biogeographic patterns. Variability in life history strategies among taxa may be influenced by biological, environmental, or phylogenetic factors, or a combination of these. While most prior research has examined these factors singularly, my aim was to investigate the effects of a host of intrinsic, extrinsic, and historical factors on two fundamental aspects of life history: egg size and egg number. I used phylogenetic generalized least-squares regression models to examine relationships between these two egg traits and a variety of hypothesized intrinsic and extrinsic variables. Adult shell morphology and spatial variability in productivity and salinity across a species geographic range had the strongest effects on egg diameter and number of eggs per capsule. Phylogeny had no significant influence. Developmental mode in Conus appears to be influenced mostly by species-level adaptations and niche specificity rather than phylogenetic conservatism. Patterns of egg size and egg number appear to reflect energetic tradeoffs with body size and specific morphologies as well as adaptations to variable environments. Overall, this series of studies highlights the importance of organism-scale biotic and abiotic interactions in evolutionary patterns.

Recombination is the process in which genetic material is exchanged between one's homologous chromosome pairs during egg or sperm development (meiosis). Recombination is necessary for proper segregation of chromosomes during meiosis, and also plays a role in purging deleterious mutations, accelerating adaptation, and influencing the distribution of genomic features over evolutionary time. While recombination is clearly an important process, recombination rate is known to vary within and between individuals, populations, and species. Furthermore, what causes this variation remains relatively unknown. Using empirical and sequenced based estimates of recombination rate for the closely related species Drosophila pseudoobscura and Drosophila miranda, I seek to understand where recombination happens across the genome, to what extent recombination changes between species, and what genomic features are responsible for these changes. These data will deepen our understanding of mechanisms determining the recombination landscape, and shed light on generalized patterns and exceptions of recombination rate variation across the tree of life.

At the end of the nineteenth century Charles Sanders Peirce wrote that "chance begets order" - indeterministic or `chancy' processes can underlie orderly and seemingly deterministic processes. Indeed, Peirce argues that indeterminism is the seed of all order in the natural world. The dissertation explores this theme in three parts. The first chapter reconstructs and elaborates Peirce's objections against necessitarianism, the position that all natural laws are perfectly orderly, deterministic. The second chapter examines and elaborates Ronald Aylmer Fisher's sophisticated analogy between gas models from statistical mechanics and his own population genetics models. The final chapter treats a contemporary indeterministic account of biological fitness and examines several points on which intuitions from deterministic theories misinterpret this quintessentially indeterministic position. The dissertation motivates an indeterministic theory of natural law and reinvigorates its implications for hierarchical models of the natural world.

The following thesis addresses an issue in ways of knowing that is both commonand destructive in the contemporary American context. Specifically, the issue of misunderstood anthropologies is posited to be an unnecessary destructive force against American churches already in decline. This damage is caused by wooden and polarizing theological and evolutionary anthropologies that underlie the basis of how many define themselves. This project endeavors to show that theological and evolutionary anthropologies are not necessarily adversarial. To this end, the theological anthropology of Gregory of Nyssa as described in On the Making of Man (de Hominis Opificio) and the evolutionary anthropology as described by Charles Darwin in The Descent of Man are defined and compared. These seminal yet still authoritative works are shown to be making different statements about humanity’s coming into being, more so than confrontational ones. The lack of mutual exclusivity between these two anthropologies is heightened by a number of interesting points of connection between them, such as reason being the definitive characteristics of humanity as well as the notion that humanity is continually becoming a more good creature. These ideas will serve to remove barriers of belief for many, all the while providing for a more holistic view of the origins of humanity and thus humanity’s place in the world.

A major goal of biological studies is to understand how complex forms develop and evolve. Each form is the result of molecular developmental patterning, growth, and the accumulation of changes in these processes from internal and external perturbations in ancestral forms. This dissertation uses each of these lenses to investigate the complex forms in the insect family Membracidae, which arises from the pronotum. In most insects, the pronotum is a simple, domed structure just behind the head, but in membracids it has enlarged and elaborated to look like thorns, plant stipules, fungi, and ants, among other shapes. To investigate this diversity, I rely on landmark based geometric morphometrics to quantify pronotal shapes. The specimens I used included those from a laboratory colony, those collected in and around San Jose, Costa Rica, and those from the Smithsonian National Museum of Natural History collection. In Chapter 1, I examined 5th instar morphogenesis to elucidate the timing of developmental events during the transition from juvenile to adult. These findings informed Chapter 2, which revealed developmental mechanisms related to growth led to transcriptional similarity between the pronotum and wings. In Chapter 3, I identified ontogenetic changes in the patterning of membracid pronotal shape compared to that of a closely related outgroup. Finally, in Chapter 4, I used a phylogenetic framework to investigate developmental modules and the co-occurrence of pronotal shape with two life history characteristics.

The process by which a single cell develops into a complex multicellular organism with specified cell types and well-defined cellular roles is not completely understood, and the evolution of that process is even more enigmatic. In sea urchin embryos, cell fate specification and differentiation of cell types occurs through gene regulatory networks, or circuits of nodes or genes that interact with and regulate each other’s DNA elements. However, what remains unclear is how a highly conserved developmental GRN can change over evolutionary time and how that can result in altered embryonic form and function.To begin to understand these processes, we developed methods to compare two relatively simple, yet complex sea urchin embryos with radically different life history strategies, the planktotrophic (conserved) Lytechinus variegatus and lecithotrophic (derived) Heliocidaris erythrogramma. To do this, single cell RNA sequencing methods were developed and adapted for the two species to address to what degree the developmental gene regulatory network genes were present, or altered when compared with the known planktotrophic dGRN. Developmental GRN information and gene signatures were applied to assign cell identities, and were vital to the identification of prospective co-expressed candidate dGRN nodes that could participate in a developmental context. With developmental atlases completed in the two species and dGRN nodes examined in both, we then compared gene signatures and dGRN nodes directly to identify prospective candidate dGRN nodes that could participate in the evolution of specification processes. We identified various novel candidates for dGRN analysis and found that, despite the obvious morphological differences, most of the dGRN circuits were conserved. In particular, we found that general specification events are delayed in Heliocidaris erythrogramma; this delay is especially prominent in the skeletogenic precursors, and the number of cells present is greatly reduced—by a factor of 10. In addition, the order of cell specification events, as shown by gene signatures, developmental sub clustering, and integrated analyses, indicate that pigment cells are among the first cell types to be specified, a finding in sharp contrast to known planktotrophic developers. Lastly, this work creates a unified framework of sea urchin development using a novel integrated model based on 1:1 gene orthologs. The application of single cell RNA-seq is a highly useful technique; when applied to a single developmental time series, it can yield insight into the genes and networks deployed over developmental time. Further, when applied to a second developmental time course, it becomes possible to uncover information about the evolution of development, as this application allows us sharp discernment into the genes and networks deployed over evolutionary time.

Searches for the genetic underpinnings of uniquely human traits have focused on human-specific divergence in conserved genomic regions, which reflects adaptive modifications of existing functional elements. However, the study of conserved regions excludes novel functional elements that descended from previously neutral regions. In this work, I integrate comparative genomic analyses with human population variation data to reveal that rapid divergence rate is associated with positive selection in human evolutionary history. Encouraged by this finding, I identified 1581 Human Ancestor Quickly Evolved Regions (HAQERs), which represent the fastest-evolved regions of the human genome. HAQERs rapidly diverged in an episodic burst of directional positive selection prior to the human-Neanderthal split before transitioning to constraint within hominins. HAQERs are enriched for bivalent chromatin states, particularly in gastrointestinal and neurodevelopmental tissues, and genetic variants linked to neurodevelopmental disease. I led a collaborative effort to develop scSTARR-seq as a multiplex single-cell in vivo enhancer assay to discover that rapid sequence divergence in HAQERs generated hominin-unique enhancers in the developing cerebral cortex. I propose that a lack of pleiotropic constraints and elevated mutation rates poised HAQERs for rapid adaptation and subsequent susceptibility to disease.

Humans are paradoxical in their ability for extreme kindness and cruelty. The goal of this dissertation is to further uncover the psychological mechanism(s) that allow humans to accept harm directed at members of other groups. The human self-domestication hypothesis proposes that human unique forms of mentalizing evolved as a byproduct of selection for ingroup prosociality. Hare (2017) proposed that late in human evolution Homo sapiens bonded more closely with ingroup members and more skillfully read the mental states of others. Moral and cultural behaviors expanded, and modern human behavior emerged. However, more closely bonded groups tend to perceive outgroup strangers as more threatening. It became advantageous to deny some forms of human-unique mental states to individuals from threatening groups. In this way emotional and moral constraints on violence toward other humans can be escaped. The potential for lethal aggression and harm toward outgroup strangers became even more extreme as a result. According to this model there should be strong psychological links between group identity, mental state attribution, moral exclusion, and a willingness to harm others. Two main mechanisms have been proposed to provide this link. The first is dehumanization or the ability to deny fully human emotions and mental abilities to another person or group of people (Haslam, 2006). The second is social dominance orientation or the perception of a hierarchy between different human groups (Sidanius & Pratto, 2001). Together these mechanisms can override individual characteristics that lead to concern. Group identity alone can be used to indicate inferiority or less than human status. Moral exclusion and harm can follow. More recently a third moderating factor has been proposed. Costello & Hodson (2010) proposed that beliefs about animals strongly shape tendencies to dehumanize. Seeing animals as having human-like minds negates the negative impact of dehumanization since being nonhuman is so similar to being human. In Chapter 1, I combine this evolutionary model with the proposed mechanisms that drive the worst forms of group-based aggression to propose the Dehumanization of Inferior Groups (DIG) Hypothesis. The DIG hypothesis suggests the perception of other groups of humans is strongly modulated by how we view the minds of other animals, their relationship with each other and our relationship to them. Our minds evolved to distinguish between humans and animals, but we develop the ability to categorize some members of our own species as more animal-like. We also evolved to categorize the relative equality or inequality of different groups. This includes groups of animals that can be perceived as different but equal or ranked hierarchically. How we perceive different groups of animals will relate to how hierarchically we view different groups within our own species. The present dissertation seeks to provide initial tests of the DIG hypothesis. To do so, I used experiment-based surveys, investigating behavioral patterns of adults and school age children. In Chapter 2, I assessed dehumanizing tendency in adults and children, revealing that variety of humanness representations can elicit dehumanization in both age groups. Similar to the links seen in previous investigations of adults, children’s willingness to dehumanize is related to their acceptance that other groups can be inferior and more deserving of punishment. In Chapter 3, I examined the association between the perception of animal-to-human similarity and dehumanization. Results in adults and children showed that highlighting mental similarities between animals and humans could narrow down the perceived animal-human divide. However, in both age group, this manipulation does not attenuate dehumanization or the intergroup biases associated with it. Chapter 4 explored the association between the treatment of other human groups and the treatment of animals in a variety of participants who were engaged in different relationship with animals. I found that people who endorsed discrimination of dog breeds also endorsed group-based discrimination in human society. Moreover, positive contact with dogs is associated with disapproval of group-based inequality. Together, these findings suggest that the perception of human intergroup relations and the perception of relationship among animal groups are dependent upon similar cognitive processes. The studies presented here have implications for understanding psychological origins of dehumanization as well as designing interventions to promote intergroup tolerance.

Environmentally cued development is widespread across the natural world. Many organisms rely on abiotic and biotic cues to undergo developmental transitions like budburst, flowering, and mating at the appropriate times of year. The study of the timing of these transitions is known as phenology. Because the timing of development determines the environment experienced by the next life history stage, it has the potential to affect evolutionary processes that occur after development. Further, because the timing of development can filter the environment experienced by the next life history stage, it can be considered a form of “habitat tracking.” In this dissertation, I use manipulative laboratory and field experiments to quantify how germination phenology can alter the postgermination environment, show that the postgermination environment can itself be genetically determined, show that germination phenology is a form of habitat tracking, and test how germination phenology can affect trait expression, natural selection, and fitness.

In my first chapter, using the ecological and genetic model species Arabidopsis thaliana, I showed that when the timing of development is genetically controlled, and the timing of development affects the environment experienced by the next developmental stage, then the environment experienced after development can itself be inherited and can evolve. Further, I demonstrated that germination phenology is a form of “habitat tracking”, by enabling seeds to establish seedlings in a subset of the full environmental conditions available. In my second chapter, using ecologically diverse A. thaliana genotypes, I show that the timing of germination can affect natural selection on postgermination traits, and that postgermination traits can affect selection on germination phenology. In my third chapter, using two plants native to North Carolina, Phacelia purshii and P. fimbriata, I show that populations can vary naturally in their propensity to germinate in response to different environmental cues, that populations preferentially germinate in habitats that are beneficial for seedlings, and when placed in new geographic locations, populations may use phenology to track novel but beneficial environmental conditions.

My dissertation placed the common process of cued development into the well- established theoretical framework of habitat tracking and habitat selection. By doing so, I was able to generate and test novel predictions about potential consequences of phenological cueing that have not yet been explored—namely, that the post- development environment itself can be inherited, that the magnitude and frequency of natural selection can vary with changes in habitat tracking, that habitat tracking itself may evolve in response to traits expressed and environments experienced after development, and that habitat tracking through phenology may be an important mechanism that organisms can use to cope with climate change.

Animal bacterial symbioses are pervasive and underlie the success of many groups. Here, I study ecological and evolutionary factors that shape interactions between a host and gut associates. In this dissertation, I interrogate interactions between the carpenter ant (Camponotus) and its associated gut microbiota to ask the following questions: What are the resident microbiota of the Camponotine gastrointestinal tract? How does persistent gut association affect rates of molecular evolution in gut symbionts? How are gut microbiota transmitted between social hosts? How does gut community composition and structure vary across host development? What evolutionary factors facilitate adaptation to the gut? How do the genomes of gut associates respond to selective pressures associated with persistent gut habitation? I use a combination of next generation sequencing, anaerobic isolate culturing, computational modeling, and comparative genomics to illustrate evolutionary consequences of persistent host association on the genomes of gut associates. In chapter one, I characterize the gut community of C. chromaiodes and describe two novel lineages in the Acetobacteraceae (AAB). I demonstrate rapid evolutionary rates, deleterious evolution at 16S rRNA, and deep divergence of a monophyletic clade of ant associated AAB. In chapter two, I design a novel molecular tool to prevent amplification of nontarget DNA in 16S based community screens. I then use this tool to characterize the gut microbiota of C. chromaiodes across several developmental stages and incipient colonies. I argue that highly similar bacterial profiles between a colony queen and offspring are indicative of reliable vertical transmission of gut bacteria. In chapter three, I isolate and culture two strains of AAB gut associates from C. chromaiodes, as well as an associate in the Lactobacillaceae, and perform whole genome sequencing. I use comparative genomic analyses to delineate patterns of genomic erosion and rampant horizontal gene transfer on AAB gut isolates that lead to genomes with mosaic metabolic pathways.

Taken together, this dissertation establishes a new model system for assessing evolutionary consequences of symbioses with gut bacteria. These results provide novel insights into the repercussions of bacterial adaptation to a host gut tract. They establish a foundation to interrogate questions unique to persistent extracellular gut symbionts. Finally, they delineate distinct forces shaping the functional capacity of symbiont genomes: gene loss through reductive evolution and gene acquisition via horizontal transfer from diverse community members.

Islands have been the inspiration for some of evolutionary biology's most important advances. This is largely due to the unique properties of islands that promote the differentiation of island species from their mainland counterparts. Rodents are widely distributed across even the most remote islands, a rarity among mammals, making them uniquely suited to study the factors leading to the divergence of insular species. In this dissertation, I use two case studies to examine the morphological and genetic divergences that take place in an insular environment.

In chapters one and two, I examine how different factors influence insular body size change in rodents. In chapter one, I examine factors influencing the direction of island body size change using classification tree and random forest (CART) analyses. I observe strong consistency in the direction of size change within islands and within species, but little consistency at broader taxonomic scales. Including island and species traits in the CART analyses, I find mainland body mass to be the most important factor influencing size change. Other variables are significant, though their roles seem to be context-dependent.

In chapter two, I use the distributions of mainland rodent population body sizes to identify `extreme' insular rodent populations and compare traits associated with those populations and their islands with those island populations of a more typical size. I find that althought there is no trend among all insular rodents towards a larger or smaller size, `extreme' populations are more likely to increase in size. Using CART methods, I develop a predictive model for insular size change that identifies resource limitations as the main driver when insular rodent populations become `extremely small'.

Chapters three and four shift their focus to a single rodent species, the deer mouse Peromyscus maniculatus, as they examine the genetic differentiation of deer mice across the California Channel Islands and the nearby mainland. In chapter three, I sequence a region of the mitochondrial control region for individuals from 8 populations across the northern Channel Islands and two mainland sites, and I analyze these sequences by calculating population genetics parameters and creating a Bayesian inference tree and a statistical parsimony haplotype network. All of these analyses reveal significant divergences between island and mainland populations. Among the islands, Santa Barbara and Anacapa islands both display unique genetic signatures, but the other northern islands remain relatively undifferentiated.

In chapter four, I genotype individuals from the previous chapter at 5 microsatellite loci, I calculate additional population genetics parameters and I utilize a Bayesian clustering algorithm to examine the similarities and differences between nuclear and mitochondrial analyses. I find the nuclear data to be largely congruent with the mitochondrial analyses; there are significant differences between island and mainland populations, and Anacapa Island is significantly differentiated from the other islands. Unlike the previous analyses, Santa Barbara Island is not significantly different from the northern islands, yet San Miguel Island has a unique genetic signature.

These studies underscore the importance of ecological processes and historical biogeography in the generation of diversity, and they highlight the role of islands as drivers of evolutionary divergence.