Browsing by Subject "Animal behavior"
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Item Open Access A Comparative Study of Habitat Complexity, Neuroanatomy, and Cognitive Behavior in Anolis Lizards(2012) Powell, Brian JamesChanging environmental conditions may present substantial challenges to organisms experiencing them. In animals, the fastest way to respond to these changes is often by altering behavior. This ability, called behavioral flexibility, varies among species and can be studied on several levels. First, the extent of behavioral flexibility exhibited by a species can be determined by observation of that species' behavior, either in nature or in experimental settings. Second, because the central nervous system is the substrate determining behavior, neuroanatomy can be studied as the proximate cause of behavioral flexibility. Finally, the ultimate causation can be examined by studying ecological factors that favor the evolution of behavioral flexibility. In this dissertation, I investigate behavioral flexibility across all three levels by examining the relationship between habitat structure, the size of different structures within the brain and total brain size, and behavioral flexibility in six closely-related species of Puerto Rican Anolis lizards. Anolis lizards provide an excellent taxon for this study as certain species, including those used here, are classified as belonging to different ecomorphs and are morphologically and behaviorally specialized to distinct structural habitat types.
In order to determine the presence of behavioral flexibility in Anolis, I first presented Anolis evermanni with a series of tasks requiring motor learning and a single instance of reversal learning. Anolis evermanni demonstrated high levels of behavioral flexibility in both tasks.
To address the pattern of brain evolution in the Anolis brain, I used a histological approach to measure the volume of the whole brain, telencephalon, dorsal cortex, dorsomedial cortex, medial cortex, dorsal ventricular ridge, cerebellum, and medulla in six closely-related species of Puerto Rican Anolis lizards belonging to three ecomorphs. These data were analyzed to determine the relative contribution of concerted and mosaic brain evolution to Anolis brain evolution. The cerebellum showed a trend toward mosaic evolution while the remaining brain structures matched the predictions of concerted brain evolution.
I then examined the relationship between the complexity of structural habitat occupied by each species and brain size in order to determine if complex habitats are associated with relatively large brains. I measured brain volume using histological methods and directly measured habitat complexity in all six species. Using Principal Component Analysis, I condensed the measures of habitat structure to a single variable and corrected it for the scale of each lizard species' movement, calling the resulting measurement relevant habitat complexity. I tested the relationship between relative volume of the telencephalon, dorsal cortex, dorsomedial cortex, and whole brain against both relative habitat complexity and ecomorph classification. There was no relationship between the relative volume of any brain structure examined and either relevant habitat complexity or ecomorph. However, relevant habitat complexities for each species did not completely match their ecomorph classifications.
Finally, I tested the levels of behavioral flexibility of three species of Anolis, A. evermanni, A. pulchellus, and A. cristatellus, belonging to three distinct ecomorphs, by presenting them with tasks requiring motor and reversal learning. Anolis evermanni performed well in both tasks, while A. pulchellus required more trials to learn the motor task. Only a single Anolis cristatellus was able to perform either task. Anolis evermanni displayed lower levels of neophobia than the other species, which may be related to its superior performance.
In combination, this research suggests that Anolis of different ecomorphs display different levels of behavioral flexibility. At the proximate level, this difference in behavioral flexibility cannot be explained by changes in the relative size of the total brain or brain structures associated with cognitive abilities in other taxa. At the ultimate level, the size of the brain and several constituent structures cannot be predicted by habitat complexity. However, behavioral flexibility in certain tasks may be favored by utilization of complex habitats. Flexibility in different tasks is not correlated, rendering broad comparisons to a habitat complexity problematic.
Item Open Access A Computational Synthesis of Genes, Behavior, and Evolution Provides Insights into the Molecular Basis of Vocal Learning(2012) Pfenning, Andreas RVocal learning is the ability modify vocal output based on auditory input and is the basis of human speech acquisition. It is shared by few distantly related bird and mammal orders, and is thus very likely to be an example of convergent evolution, having evolved independently in multiple lineages. This complex behavior is presumed to require networks of regulated genes to develop the necessary neural circuits for learning and maintaining vocalizations. Deciphering these networks has been limited by the lack of high throughput genomic tools in vocal learning avian species and the lack of a solid computational framework to understand the relationship between gene expression and behavior. This dissertation provides new insights into the evolution and mechanisms of vocal learning by taking a top-down, systems biology approach to understanding gene expression regulation across avian and mammalian species. First, I worked with colleagues to develop a zebra finch Agilent oligonucleotide microarray, including developing programs for more accurate annotation of oligonucleotides and genes. I then used these arrays and tools in multiple collaborative, but related projects, to measure transcriptome expression data in vocal learning and non-learning avian species, under a number of behavioral paradigms, with a focus on song production. To make sense of the avian microarray data, I compiled microarray data from other sources, including expression analyses across over 900 human brain regions generated by Allen Brain Institute. To compare these data sets, I developed and performed a variety of computational analyses including clustering, linear models, gene set enrichment analysis, motif discovery, and phylogenetic inference, providing a novel framework to study the gene regulatory networks associated with a complex behavior. Using the developed framework, we are able to better understand vocal learning at different levels: how the brain regions for vocal learning evolved and how those brain regions function during the production of learned vocalizations. At the evolutionary level, we identified genes with unique expression patterns in the brains of vocal learning birds and humans. Interesting candidates include genes related to formation of neural connections, in particular the SLIT/ROBO axon guidance pathway. This algorithm also allowed us to identify the analogous regions that are a part of vocal learning circuit across species, providing the first quantitative evidence relating the human vocal learning circuit to the avian vocal learning circuit. With the avian song system verified as a model for human speech at the molecular level, we conducted an experiment to better understand what is happening in those brain regions during singing by profiling gene expression in a time course as birds are producing song. Surprisingly, an overwhelming majority of the gene expression identified was strongly enriched in a particular region. We also found a tight coupling between the behavioral function of a particular region and the gene expression pattern. To gain insight into the mechanisms of this gene regulation, we conducted a genomic scan of transcription factor binding sites in zebra finch. Many transcription factor binding sites were enriched in the promoters of genes with a particular temporal patterns, several of which had already been hypothesized to play a role in the neural system. Using this data set of gene expression profiles and transcription factor binding sites along with separate experiments conducted in mouse, we were able uncover evidence that the transcription factor CARF plays a role in neuron homeostasis. These results have broadened our understanding of the molecular basis of vocal learning at multiple levels. Overall, this dissertation outlines a novel way of approaching the study of the relationship between genes and behavior.
Item Open Access Aspects of the Feeding Ecology of the Antillean Manatee (Trichechus manatus manatus) in the Wetlands of Tabasco, Mexico(2013) GonzalezSocoloske, DanielManatees (Mammalia: Sirenia), along with the closely related dugongs, are the only herbivorous marine mammals. Manatees consume a wide variety of vascular plants and algae in both marine and freshwater habitats. However, little is known about what characteristics influence diet and food selectivity, especially in freshwater habitats, which represent a large portion of the available habitat for the endangered Antillean manatee, Trichechus manatus manatus, in Central and South America. Understanding foraging ecology is an important element of effective conservation strategies.
This dissertation investigated various aspects of the foraging ecology of the Antillean manatee in a freshwater habitat, specifically: 1) how plant availability (i.e. species richness, diversity, and abundance) varied seasonally with changes in water depths, 2) manatee food selectivity from a representative set of plant species from that freshwater habitat, and 3) the relationship of plant nutritive compounds and availability with manatee food selectivity. In addition, this dissertation describes the multiple uses of sonar technology for studying manatees and habitat characteristics in freshwater.
Plant availability to manatees was evaluated by conducting monthly plant surveys from July 2010-July 2011 in four contact lakes in the wetlands of Tabasco, Mexico. Manatee food selectivity was examined by conducting food selection experiments on a wild adult manatee during the low water season with 54 plant species representing 25+ genera. The nutritive components (i.e. crude protein (CP), neutral detergent fiber (NDF), acid detergent fiber (ADF), hemicellulose (HC), and ash) and plant availability values for selected and non-selected plants species were evaluated to determine their relationship with manatee food selectivity. The applicability of using side-scan sonar for manatee research was tested in various freshwater and estuarine habitats in Honduras, Costa Rica, Panama, and the wetlands of Tabasco, Mexico between 2006-2011.
The major findings of this dissertation are as follows. Plant species richness, diversity, and abundance were greatest during the rising water season (July-August) and lowest during the low water season (March-June). No plants were available in April-June, which represented the majority of the low water season. The wild manatee
selected 27 (11+ genera) of the 54 species examined during the feeding experiments. Of the plant characteristics tested (i.e. nutritive components and plant availability), only digestible fiber (HC) was significantly related to manatee food selection, with manatees
selecting plants with higher HC content. Four unique applications were identified for the use of side-scan sonar to facilitate manatee research in freshwater habitats: 1) confirmation of visual sightings and determination of group size, 2) determination of mother-calf pairs, 3) habitat characterization, and 4) assisting manatee captures.
Results from this study reveal that manatees living in the freshwater wetlands of Tabasco, Mexico have to cope with a highly seasonal availability of plants and that while manatees consume plants from a wide variety of genera, they are highly selective. Unlike other herbivorous mammals, manatee food selectivity was not influenced by CP, NDF, or ADF, but rather by digestible fiber. A unique suit of anatomical and physiological characteristics suggests that manatees may be fiber digestion specialists. Both seasonal plant availability and the manatee's large dietary breadth must be considered when developing 1) conservation strategies for wild manatees in freshwater habitats and 2) protocols for captive rehabilitation of orphaned and stranded manatees that will be reintroduced into the wild.
Item Open Access Drones and Machine Learning for Marine Animal Behavior Analysis(2023-04-28) Poling, DavidUnderstanding the behavior of marine animals is critical to effective management especially as they fall under increasing anthropogenic pressures. Recent advances in two technologies, drones and machine learning offer versatile, data driven, automatable solutions capable of effective collection and analysis of large datasets. In this paper I illustrate how pose estimation as an effective machine learning based solution for analyzing marine animal behavior. This study investigates pose estimations use on drone imagery due to its rising prevalence in marine science and prior combination with pose estimation in our lab. As initial work at our lab has investigated the use of pose estimation on marine mammal datasets and my goal is to expand on these efforts and build an overview of both technologies integration for researchers interested working with them. In the present study I use a collection of shark video taken by myself and other Duke researchers locally off the Rachel Carson Reserve on the North Carolina coast as demonstration and to help build a catalog of models and best practices for use of pose estimation on different taxa. This paper will provide an overview of drones and pose estimation including Social LEAP Estimates Animal Poses (SLEAP), a pose estimation framework which has proven to have good potential in marine science. SLEAP was chosen due to its accessibility, versatility and tracking algorithm which allows multiple subjects to be tracked and analyzed at the same time. The latter is a major steppingstone for pose estimation software as past projects may have been able to identify multiple individuals in one frame but not be able to keep track of who is who across thousands of frames of video. Covered topics will include: 1. Technical overview of drones and pose estimation. 2. Data collection 3. Using pose estimation a. Model types and programming 4. Data export and processing 5. Analysis 6. Conclusions on using pose estimation in marine science and future work. After data export, a novel solution will also be assessed for compensating for camera movement, in this case a moving drone, which has proven to be one of the biggest roadblocks of using SLEAP, which was developed for processing stationary video. This solution processes data in a way that is plug and play with existing analytical methods and will be open source.Item Open Access Exploring the Impacts of Major Histocompatibility Complex Variation on Fitness in the Ring-tailed Lemur (Lemur catta): Parasite Resistance, Survival, Mate Choice and Olfactory Ornamentation, and Reproduction(2014) Grogan, Kathleen ElizabethThe threats of human encroachment and climate change are increasing and understanding the interplay between genetic diversity, fitness, and ecological variation has become critical for predicting adaptive responses and species extinction risk. Decreasing genetic diversity, owing to population decline or inbreeding, can be detrimental at the level of the individual, population, or species. One of the major challenges for evolutionary and conservation biologists is identifying the specific genetic components that influence inter-individual variation in fitness remains. As a direct link between genetic-make up and individual fitness, the Major Histocompatibility Complex (MHC) is critical to the activation of the adaptive immune system. Biologist have suggested that in addition to influencing an individual's health, variation at the MHC may be related to an individual's survival and reproductive success. Here, I test this hypothesis using two populations of ring-tailed lemurs (Lemur catta) at long-term study sites to achieve individual and population-level comparisons of MHC diversity and to integrate new genetic technology with behavioral, ecological, and environmental data. First, I address the difficulty of genotyping large populations at hypervariable genes by using next generation sequencing and suggest improvements to current methods. Second, I describe patterns of variation at the MHC-DRB 2nd exon, including diversity between alleles, individuals, and populations. Next, I examine the relationship between MHC-DRB diversity and measures of immunocompetence, parasitism, and survival within a broader framework of ecological variability across captive and wild conditions. Because the MHC is also thought to be important in mate choice and reproduction, I use an experimental approach in captive individuals to investigate possible mechanisms of MHC-based signaling through olfactory communication. Lastly, I link a female's MHC genotype to her reproductive success in the wild and explore if this relationship is altered by environmental stressors. The results of this dissertation emphasize the increasing feasibility of using genetic approaches to investigate the fitness correlates of genetic diversity non-model systems. These advances are critical for future studies and the integration of behavioral, ecological, and genetic perspectives in semi-natural and wild environments.
Item Open Access Fine-Scale Foraging Behavior of Humpback Whales Megaptera novaeangliae in the Near-Shore Waters of the Western Antarctic Peninsula(2014) Tyson, Reny BlueHigh-resolution bio-logging tools were used to examine the fine-scale foraging behaviors of humpback whales (Megaptera novaeangliae) in the coastal waters of the Western Antarctic Peninsula during the austral autumn of 2009 and 2010. Discrete feeding events (i.e., lunges) were inferred from the biologging records of thirteen whales, including a mother and her calf. In general, humpback whales exhibited efficient foraging behaviors that allowed them to maximize energetic gains and minimize energetic costs as predicted by optimal foraging theory. They fed at a continuous and high rate in the upper portion of the water column (< 100 m) from approximately dusk to dawn when their prey (Antarctic krill, Euphausia superba) were most vulnerable and less costly to acquire (i.e., near the surface). When forced to dive to greater depths, they adjusted their behaviors (e.g., descent and ascent rates) so that they could maximize their foraging durations and increase their lunging rates. In addition, humpbacks appeared to accept short term (i.e., dive by dive) costs associated with depleted oxygen stores in favor of maximizing long term (i.e., daily) energetic gains. Such efficient behaviors are particularly beneficial for mother-calf pairs who have additional energetic costs associated with foraging, such as lactation (mother), growth (calf), and maintaining proximity. In addition, because the physiology of humpback whales is poorly understood yet critically important for predicting their behaviors in response to fluctuations in their environmental conditions, foraging behaviors inferred from the bio-logging records were used to estimate their metabolic rates, oxygen storage capacities, and oxygen replenishment rates under the framework of optimal foraging theory. This research suggests that the current techniques used to estimate humpback whale oxygen stores is appropriate but that the estimation of metabolic rates of humpbacks while foraging and while traveling need to be addressed further. This work aims to increase the current understanding of humpback whale foraging behaviors along the Western Antarctic Peninsula so that appropriate measures can be taken to aid in their recovery and in the sustainability of the Antarctic marine ecosystem.
Item Open Access Foraging for Information in the Prefrontal Cortex(2014) Adams, Geoffrey KeithThe ability to monitor, learn from, and respond to social information is essential for many highly social animals, including humans. Deficits to this capacity are associated with numerous psychopathologies, including autism spectrum disorders, social anxiety disorder, and schizophrenia. To understand the neural mechanisms supporting social information seeking behavior requires understanding this behavior in its natural context, and presenting animals with species-appropriate stimuli that will elicit the behavior in the laboratory. In this dissertation, I describe a novel behavioral paradigm I developed for investigating social information seeking behavior in rhesus macaques in a laboratory setting, with the use of naturalistic videos of freely-behaving conspecifics as stimuli. I recorded neural activity in the orbitofrontal and lateral prefrontal cortex of monkeys as they engaged in this task, and found evidence for a rich but sparse representation of natural behaviors in both areas, particularly in the orbitofrontal cortex. This sparse encoding of conspecifics' behaviors represents the raw material for social information foraging decisions.
Item Open Access Genomic and Phenotypic Consequences of Hybridization in Wild Baboons(2022) Fogel, Arielle SarineHybridization, the process of interbreeding between distinct taxa, was once thought to be rare in animals. However, in the past two decades, new data have challenged this paradigm. Ancient and/or ongoing hybridization has now been documented in a wide variety of animals, including in our own lineage. A key puzzle that emerges from these observations is that despite the pervasiveness of hybridization, many species nevertheless remain distinct. My dissertation addresses this puzzle by integrating long-term field data on morphology, behavior, demography, and ecology with newly generated genomic data from a natural hybrid zone between yellow baboons (Papio cynocephalus) and anubis baboons (P. anubis) in Kenya.
My work addresses three main themes: (i) the effects of ancestry on fitness-related traits in hybrid zones; (ii) the role of behavior in mediating gene flow between species; and (iii) the genomic signature of natural selection post-hybridization. I show that genetic ancestry predicts male-female social bonds, a predictor of lifespan in this population. Animals with more introgressed ancestry (i.e., genetic regions transferred via hybridization) are more likely to affiliate with the opposite sex, and pairs of animals with similar ancestry show an increased propensity for affiliation. These findings suggest that affiliative behavior may simultaneously promote and constrain baboon hybridization, through additive and assortative effects of ancestry, respectively. My research also rules out the possibility that fetal loss—a major cost to female fertility—acts as a strong isolating barrier. Fetal loss is independent of maternal genetic ancestry; instead, age and ecological stressors are the main determinants of pregnancy outcomes in baboons. Notably, although these analyses fail to identify clear costs to hybrid ancestry, population genomic evidence points to selection against introgression in baboons, suggesting subtle but important phenotypic effects of ancestry that have yet to be revealed. Finally, I identify specific regions of the baboon genome that may serve as barriers to gene flow. A subset of these genomic regions may explain ancestry-based assortative mating behavior in the hybrid zone. Together, my work demonstrates how hybridization has shaped the genomes and phenotypes of interbreeding baboons. It also provides a much-needed comparative perspective against humans, illuminating the shared and distinctive features of admixture as an evolutionary process in human evolution, and more broadly reveals how primates fit into our changing concept of animal evolution more broadly.
Item Open Access Integrating Multiple Technologies to Understand the Foraging Behavior and Habitat Use of Monk Seals in the Main Hawaiian Islands(2015) Wilson, Kenady ColleenHawaiian monk seal abundance is currently declining by about 4% per year with current population estimates around 1,100 individuals. Although the overall population continues to decline, a small sub-population in the main Hawaiian Islands (MHI) appears to be increasing by roughly 6% per year. Monk seal conservation and recovery efforts in the MHI have been hindered by the perception that seals do not belong there, and that they compete with fisheries and damage coral reefs. Education and outreach efforts describing the actual impact of monk seals in the MHI are currently underway, but we actually know very little about their at-sea behavior, especially in the MHI, even though Hawaiian monk seals have been studied extensively since the 1980s. The central objective of my dissertation was to describe monk seal behavior and develop a baseline for monk seal foraging ecology and habitat use in the MHI. To accomplish this I combined three-axis accelerometers, National Geographic Crittercams, and GPS tags to study monk seal foraging behavior. I instrumented 16 seals between 2010 and 2014 on the islands of Molokai, Kauai, and Oahu and deployed an additional 24 GPS tags without the accelerometer and Crittercam. I recovered each Crittercam/accelerometer package 3-6 days after deployment, resulting in an average of 6.14 hours of video footage per seal. The GPS tags continued to record data for 3-6 months providing long-term summaries of dive and haul-out behavior. Using a Bayesian framework I modeled monk seal behavior and habitat use, and developed a method to identify feeding events from accelerometer data. There was a high level of individual variation in the movements of monk seals, but general descriptions of their behavior were accurate at the population level. On average, foraging trips lasted 0.81 ± 1.38 days and seals traveled 28.45 ± 82.03 km per trip. Most seals began benthic dives shortly after entering the water, with most dives occurring between 20-40 m. I used kernel density estimation to define the 50% (core area) and 95% (home range) utilization distribution for each seal. The median home range and core area size for seals in the MHI was 265.62 km2 and 1,564.56 km2, respectively. The pitch axis of the accelerometer was a reliable metric, with over 70% accuracy, for identifying foraging events for monk seals. Body motion over the course of a dive, and how close the seal was to the seafloor during a dive (dive ratio) were the best predictors of these foraging events. Consequently, dive ratio was used to infer foraging in long-term telemetry records that lacked concurrent accelerometer data. Analysis of these data relative to habitat preferences revealed two distinct movement modes for monk seals in the MHI: near shore and offshore/inter-island. My research developed the first thorough understanding of monk seal movements and habitat use in the MHI and provided insight into the mechanisms contributing to the behavioral variability observed for this species. I hope that a detailed understanding of the foraging behavior of monk seals will provide insight into their true role in the ecosystem and help foster the recovery of this critically endangered species.
Item Open Access Lizard Communication(2015) Steinberg, DavidThe evolution of animal signals is driven largely by characteristics of the signaling environment and properties of receiver sensory systems. Selection favors signal traits that increase the probability that a signal will stimulate the sensory systems of intended receivers, but not potential predators, under average environmental conditions. However, environmental conditions often fluctuate, which means that a given signal property may not be equally effective at all times. One potential mechanism that an organism might employ to overcome this challenge is to modulate its signal properties as environmental conditions change in order to maintain stimulation of the receiver sensory system. In this dissertation, I explore the possible role of signal modulation using the motion detection and communication systems of tropical Anolis lizards.
In order to assess the possible role of signal modulation in the communication behavior of anoles, it was necessary to determine the properties of their motion detection systems. In Chapter 2, I tested whether motion detection properties are conserved across species of anole. I adapted a behavioral assay to quantify the spatial parameters of the motion detectors of three species of Puerto Rican Anolis lizards, with each preferring a distinct structural habitat type. I then compared the results to data previously collected for anoles from Cuba, Puerto Rico, and Central America. Results indicated that all species share a minimum amplitude threshold for detecting moving objects and exhibit multiple peaks in relative response to various motion amplitudes. Fine-scale interspecific differences in the number and values of response peaks were not correlated with structural niche. Overall, the study suggests that the motion detection systems of Anolis lizards are relatively conserved, which may help explain shared features of movement-based signals in anoles.
For mobile organisms, the spatial relationships of signaling individuals and intended receivers can be fluid. Such fluctuation in the distance between signalers and receivers can greatly impact signal efficacy, but it is unclear exactly how animals cope with this problem. In Chapter 3, I investigated whether signal modulation can serve as an effective strategy to cope with variation in the spacing of receivers in the environment by tuning a signal to maintain stimulation of the receiver sensory system. I evaluated this hypothesis by testing the use of modulation in the tropical lizard Anolis gundlachi in Puerto Rico. I first characterized the motion detection properties of the sensory system of A. gundlachi in the laboratory. I then measured the physical properties of movement-based headbob displays given during staged social encounters under natural conditions. I found a significant positive association between the maximum amplitude of headbob displays and the physical distance to intended receivers. Modulation occurred in response to small-scale changes in signaler-receiver distance, and signalers gave displays that fell within a range of amplitudes predicted to optimally stimulate the visual system of A. gundlachi. These findings strongly suggest that modulation of the physical properties of motion-based signals can be an effective mechanism to tune signals to both characteristics of receiver sensory systems and receiver distance, and can serve as a behavioral strategy to cope with relatively frequent changes in the spacing of individuals.
Although signaling individuals must effectively capture and hold the attention of intended conspecific receivers, they must also limit eavesdropping by potential parasites or predators. However, predation pressure can vary over the course of an individual's lifetime, or over the course of a day, thereby altering signal efficacy. In Chapter 4, I tested the hypothesis that prey can modulate the physical properties of their signals or their display behavior in order to decrease conspicuousness and potentially limit predation risk. To do so, I conducted a manipulative experiment in nature to determine the effect of predation pressure on the properties of movement-based signals and the display rate of the semiarboreal lizard Anolis sagrei. I found that male anoles reduced the maximum amplitude of headbob displays but not the proportion of time spent signaling on islands onto which predators were introduced, in comparison to males from control islands lacking the predator. Characteristics of the motion detection system and social behavior of A. sagrei show that this reduction in amplitude also decreases signal active space, which might alter the reproductive success of signaling individuals. I suggest that future studies of predator-prey interactions consider the risk effects generated by changes in signals or signaling behavior to fully determine the influence of predation pressure on the dynamics of prey populations.
Item Open Access Molecular Causes and Consequences of Sperm Competition in Agelaius Blackbirds(2014) Liu, Irene Ai-YinSexual selection has long been framed as a process that ends when copulation is achieved. However, in species with polyandry (multiple mating by females), competition persists after mating inside the female's reproductive tract, where sperm from multiple males must then compete to fertilize a female's eggs. This post-mating process, known as sperm competition, is thought to be just as strong as the competition to secure a mate. Because sperm competition has only recently been observed, its evolutionary role remains largely unknown. In this dissertation, I use field, laboratory and computational approaches to understand the evolution of sperm competition in two ways: (1) by testing a possible source of variation in sperm competition within species, and (2) by examining how variation in sperm competition results in DNA evolution across species. My study system is the Agelaius clade of New World blackbirds, a group of songbirds with predicted variation in the intensity of sperm competition. In the first half of the dissertation, I explore the factors that affect how intensely sperm competition is experienced in a population. In Chapter 1, I assess the relationship between genetic diversity and extra-pair paternity (EPP, a proxy for sperm competition) in seven continental and one island population of red-winged blackbird (A. phoeniceus). I find that while genetic diversity varies significantly across populations, the population with the lowest amount of genetic diversity exhibits similar rates of EPP as the more diverse populations, providing no support for a relationship between genetic diversity and EPP rate. This result suggests that genetic diversity by itself is not an determining factor in EPP variation. In Chapter 2, I characterize the mating system of the endangered yellow-shouldered blackbird (A. xanthomus) and provide the first evidence that it, too, engages in EPP despite having low genetic diversity. I additionally present a conservation genetics profile of the species, showing that the yellow-shouldered blackbird's low effective population size and genetic diversity, both likely due to a recent bottleneck, may be increasing its vulnerability to extinction. I suggest ways in which future management decisions might account for the genetics of a small population. In the second half of the dissertation, I examine whether sperm competition itself can drive the molecular evolution of a species. I focus on the evolutionary patterns of seminal fluid proteins (Sfps), which are transferred with sperm during copulation and are known targets of sperm competition. I describe in Chapter 3 the transcriptomic and proteomic techniques I use to identify protein-coding genes in a non-model organism, presenting the first list of seminal fluid proteins in a songbird. I contrast the protein profile of the blackbird with the protein profile of insect and mammalian Sfps. Finally, in Chapter 4, I use eight of the proteins identified from the list to look for patterns of positive selection on these proteins. Specifically, I test whether Sfps evolve faster in species with mating systems featuring high levels of sperm competition than in species with mating systems featuring low levels of sperm competition. I first compare EPP rates measured from the previous two species with a third species, the tricolored blackbird (A. tricolor), and find that all three experience similar levels of sperm competition. From the catalog of genes derived in Chapter 3, I select, sequence and search for evidence of rapid evolution in six candidate Sfps and two control genes. I find that not only is there no evidence for positive selection in any of these genes, there is strong evidence for purifying selection and furthermore very low levels of diversity within and divergence across species. Reasons for these unexpected preliminary findings could be both microevolutionary or macroevolutionary in nature and warrant larger-scale studies, especially across a broader sample of taxa and across species with greater variation in sperm competition. Taken together, this dissertation describes the relationship between mating systems, sperm competition and post-mating adaptations. By examining the effect of mating system on protein divergence, it links sexual selection with molecular evolution while generating behavioral, genetic, transcriptomic and proteomic resources for future comparative studies.
Item Open Access Revisiting Sexual Selection: An Exaggerated Signal of Fertility in the Amboseli Baboons(2012) Fitzpatrick, CourtneySexual selection has long been accepted as a widespread force of evolution shaping male traits across taxa. In recent years, biologists have begun to investigate the extent to which sexual selection may also shape traits among females. However, current models of sexual selection have largely been developed using assumptions that--while generally met in males--often do not apply to females. Thus, attempts to apply these contemporary models to the study of sexual selection in females reveal weaknesses in the theoretical framework for sexual selection research. One consequence of this for empirical research is that researchers often infer the action of sexual selection upon evidence of male mate choice. Although male mate choice is increasingly common, it is much less likely to exert selection pressure than its female counterpart. I begin by proposing a conceptual framework that explicitly accounts for ...Next, I investigate a female trait that has recently become an iconic example of sexual selection in females; that is the exaggerated estrous swellings of cercopithecine primates. By combining morphological data collected with a non-invasive photographic method and observational behavioral data with longitudinal ecological and demographic data from the ongoing Amboseli Baboon Research Project, I examine the sources of variance in this exaggerated signal of fertility. Finally, I test the hypothesis that male baboons prefer females with larger sexual swellings because those females have higher fitness. I find no evidence to support this hypothesis. Instead, my results suggest that mate choice among male baboons has evolved to detect, not the intrinsic quality of the female as has typically been proposed, but the quality of a reproductive opportunity.
Item Open Access The Behavior and Energetics of Ritualized Weapon Use in Mantis Shrimp (Stomatopoda)(2018) Green, Patrick AndrewContests are essential parts of an animal’s life history, as they dictate access to critical resources like mates, food, or territory. Studying how animals efficiently assess competitive ability to resolve contests is a central goal of research in animal behavior. Additionally, studies of how animals use traits like signals and weapons in contests lends insight to the evolution of those traits. In this thesis, I study assessment and resolution of territorial contests – as well as the function of signals and weapons in contests – in the mantis shrimp Neogonodactylus bredini (Stomatopoda: Crustacea).
Behavioral theory predicts that animals may use visual or other displays to communicate reliable information on ability, resolving contests without the use of potentially costlier combat, such as biting, grasping, or striking with weapons. In Chapter 2, I show that N. bredini do not match these predictions – the size of structures presented during visual weapon displays did not correlate with strike performance, and almost all contests involved weapon use via high-force striking. Because most strikes were exchanged on the armored telson (tailplate), I hypothesized that the ritualized “telson sparring” behavior helps competitors avoid contest costs and functions as a signal, instead of dangerous combat.
Studies of assessment help show what information competitors use to make decisions during contests and can reveal the role specific behaviors play. In Chapter 3, I show that N. bredini use mutual assessment during both size-matched and non size-matched contests; that is, competitors gather information about both themselves and their opponent. I also show the role telson sparring and other behaviors play during this assessment.
Finally, in Chapter 4, I test how the energetic cost of delivering sparring strikes scales with body size. I find that larger competitors used proportionally more energy when striking, that this positive scaling of energy resulted in constant scaling of velocity across size, and that these results matched predictions from a mathematical model of the strike mechanism. Furthermore, I show that these scaling dynamics are different from those of strikes delivered in another behavioral context: feeding on hard-shelled prey.
Overall, this thesis shows that the use of deadly weapons in contests should not be assumed as dangerous combat; instead, I show how ritualized behaviors allow for weapon use to function in assessment. The approaches used and conclusions made from this thesis can inform work in contest behavior, functional morphology, and biomechanics.
Item Open Access The Effects of Habitat Parameters on the Behavior, Ecology, and Conservation of the Udzungwa Red Colobus Monkey (Procolobus gordonorum)(2012) Steel, RuthA central theme in animal ecology is the study of the relationship between ecology and behavior. This dissertation demonstrates how ecological parameters, particularly food and weather variables, correlate with ranging, activity budget, and diet in Udzungwa red colobus monkeys (URC, Procolobus gordonorum), endemic to the Udzungwa Mountains, Tanzania.
From April 2009 - March 2010, four URC groups were habituated and studied in Mwanihana and Magombera Forests. During all-day follows, ranging, activity budget, and diet data were collected using GPS units and ten-minute scan samples of sustained activities. Food characteristics were assessed using transect and phenology surveys. Preliminary nutritional analyses were conducted on species-specific parts fed upon during October. I designed and employed novel methods for estimating ranging statistics which were compared with conventional methods.
Home range sizes were relatively small (8.8 - 20.8 ha). Home range size may relate to food species diversity and feeding selectivity for species-specific food parts. Variability in dietary composition was partly explained by plant phenology, forest composition, and selectivity differences among groups. URC primarily fed upon young leaves with higher fat content. Some non-nutritive items eaten may function as detoxifying agents. Data suggest that the URC dietary strategy involves nutrient balancing (i.e. maximizing energetic intake and nutrient acquisition while avoiding high concentrations of particular plant secondary compounds).
Mean daily travel distance (DTD) was 970 m, longer than in other red colobus taxa. DTD was shorter in October and November when temperatures were warmer and a high abundance of young growth became available. Young growth comprised the majority of all groups' diets in each sample period. When young growth abundances were highest, Magombera groups traveled shorter distances. One group's DTD did not differ seasonally and was significantly longer compared to other groups. This group may have traveled longer distances and spent less time resting in order to consume young growth in a habitat with lower young growth abundances. A correlation between time spent resting and temperature suggests behavioral prevention of hyperthermia. URC energetic strategies may involve balancing thermoregulation with maximizing energy intake. Conservation recommendations are discussed and include stricter forest protection.
Item Open Access The Origin of Prosociality Toward Strangers(2013) Tan, JingzhiHumans are champions of prosociality. Across different cultures and early in life, humans routinely engage in prosocial behaviors that benefit others. Perhaps most strikingly, humans are even prosocial toward strangers (i.e. xenophilic). This is an evolutionary puzzle because it cannot be explained by kinship theory, reciprocal altruism or reputation. The parochialism hypothesis proposes that this extreme prosociality is unique to humans, is motivated by unselfish motivation and evolved through group selection made possible by human culture and warfare. The first impression hypothesis, on the other hand, proposes that xenophilia can evolve to promote the selfish benefits that accrue from extending one's social network. It predicts that 1) nonhuman species can evolve prosociality toward strangers when the benefit of forming new relations is higher than the cost, 2) the motivation for prosociality can be selfish, and 3) encounters with strangers can be a positive social event since strangers represent potential social partners. This dissertation presents three sets of experiments designed to test these predictions with bonobos (Pan paniscus), a species known for reduced xenophobia. These experiments showed, first, that bonobos voluntarily shared monopolizable food with a stranger and helped the stranger to obtain out-of-reach food. Second, the observed prosociality was driven by a selfish motivation to initiate an interaction with the stranger in close proximity and an other-regarding motivation to benefit the stranger. Third, an involuntary yawning task and a voluntary choice task show converging results that bonobos attribute positive valence to completely unknown strangers by default. These experiments support the three core predictions of the first impression hypothesis and challenge the view that intergroup competition is crucial to the origin of prosociality toward strangers in our species. Instead, the first impression hypothesis proposes that xenophilia in bonobos is probably an adaptation to initiating non-kin cooperation. Because female bonobos are highly cooperative even though they are the dispersing sex, xenophilia might function to quickly establish cooperative relationships with new immigrants. This suggests that xenophilia and reciprocity are likely two complementary aspects of non-kin cooperation: the former explains its initiation while the latter explains its maintenance. Similarly, xenophilia in humans is likely a result of the increasing need for cooperation among non-kin due to enhanced fission-fusion dynamics, population expansion, obligate cooperative foraging and greater dependence on cultural knowledge.
Item Open Access The Perceptual and Decision-Making Processes Guiding Species and Sex Recognition and Rival Assessment in the Jumping Spider Lyssomanes viridis(2013) Tedore, Cynthia AnneThe goal of this dissertation was to better clarify the sensory and cognitive capabilities and limitations of a size-constrained animal. Because visually-guided behaviors are more experimentally tractable than behaviors guided by other sensory modalities, I chose to study a small animal with an unusually good visual system and a suite of apparently visually-guided behaviors, the jumping spider Lyssomanes viridis (Salticidae). Jumping spiders' principal eyes, which are adapted for the perception of shape and pattern, have the highest measured acuity of any arthropod, but also the narrowest field of view, making salticids a particularly interesting study system for measuring the capabilities and limitations of a tiny animal with small yet apparently highly functional eyes. For my dissertation, I examined the amount and type of visual information gathered in high-stakes encounters; i.e. species and sex recognition and male-male contests over females. In salticids, the wrong assessment of species and sex or fighting ability carries with it the risk of injury or even death. Thus, more information, and especially high-resolution information, should be particularly adaptive in such encounters, and should provide us with a good proxy of the perceptual and cognitive capabilities and limitations of this small animal.
In chapter two, I assayed the amount and type of visual information gathered in the context of species and sex recognition, and tested for crossmodal interactions between pheromones and visual cues. Using computer-animated stimuli, I found that, although males took the time necessary to visually scan both the face and legs of other spiders before deciding whether to threaten, court, or ignore them, their conspecific visual recognition templates were fairly coarse, and resulted in them making numerous misidentifications and frequently courting heterospecific salticids. This was especially true in the presence of conspecific female pheromones. Pheromones appeared to exert further top-down effects on visual recognition of conspecifics by bringing visual recognition templates into working memory, as was inferred from the fact that males spent less time examining conspecific images in the presence of conspecific female pheromones. Pheromones also increased the probability that a non-conspecific spider bearing even a slight resemblance to a conspecific female spider would be recognized and courted as a conspecific female. However, pheromones usually did not hasten the recognition of non-conspecific images; this indicates that males' poorer recognition accuracy in the presence of pheromones was not a result of males' spending less time visually examining non-conspecific images.
In chapter three, I looked for correlations between various visual features and contest success in order to determine what types of visual information opponents could theoretically use to assess their opponents' resource holding potential in contests over females. I found that all measured size-related traits correlated strongly with contest success, but that coloration did not, except in the rare cases in which a smaller male won a contest. In these encounters, males who won, despite being smaller, had less red chelicerae than their opponents. Finally, in chapter four, I used the results of chapter three to begin assessing whether the traits that correlate with contest success are actually assessed by males, and in particular, whether they are assessed visually. To do this, I presented males with various sizes of computer-animated opponents, and found that males were less likely to threaten larger opponents. Thus, males seem to be using visual cues to gather information about the size of their opponents. Whether they evaluate overall size, or more specifically, the size of their opponents' weapons, will be addressed in future work.
Item Open Access The Psychology and Evolution of Foraging Skills in Primates(2012) Rosati, AlexandraPrimates in the wild face complex foraging decisions where they must assess the most valuable of different potential resources to exploit, as well recall the location of options that can be widely distributed. While differences in diet and ecology have long been thought to be an important factor influencing brain evolution in primates, it is less well understood what psychological abilities animals actually use when making foraging decisions. This dissertation examines cognitive domains that play a crucial role in supporting foraging behaviors--spatial memory and decision-making--by integrating both psychological and biological approaches to behavior. In particular, the research presented here examines multiple species of primates to address the cognitive skills that different animals use to solve foraging problems (at the proximate level of analysis), as well as why some species appear to solve such problems differently than other species (at the ultimate level of analysis).
The first goal of the dissertation is to compare closely-related species that vary in ecological characteristics, in order to illuminate how evolution shapes the cognitive skills used in foraging contexts. This component focuses on comparisons between chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), humans' closest extant relatives. In addition, this component reports comparisons amongst strepsirrhines (Lemur catta, Eulemur mongoz, Propithecus coquereli, and Varecia subsp.) to model cognitive evolution in a taxonomic group with greater ecological diversity than Pan. The first two chapters test the hypothesis that more frugivorous species exhibit more accurate spatial memory skills, first by comparing apes' spatial memory abilities (Chapter 2), and then by comparing four species of lemurs on a related set of spatial memory tasks (Chapter 3). In subsequent chapters, I examine apes' decision-making strategies to test the hypothesis that chimpanzees are more willing to pay decision-making costs than are bonobos, due to differences in their feeding ecology. I focus on preferences about the timing of payoffs (Chapter 4); preferences about risk, or the variability in payoffs (Chapters 4 and 5); and preferences about ambiguity, or knowledge about available options (Chapter 6).
The second goal of the dissertation is to compare the psychological mechanisms that human and nonhuman great apes use for foraging, in order to identify potentially human-unique cognitive abilities. In terms of spatial memory, I examine whether other apes also exhibit human-like patterns of spatial memory development (Chapter 2). In terms of decision-making, I examine whether apes exhibit a suite of human-like biases when making value-based choices. In particular, I test whether emotional and motivational processes, which are critical components of human decision-making, also play a role in apes' choices (Chapters 4); whether apes are sensitive to social context when making economic decisions (Chapter 5); and whether apes are sensitive to their degree of knowledge when making choices under uncertainty (Chapter 6). Finally, I directly compare human and ape preferences on a matched task to assess whether humans use any unique psychological abilities when making decisions about risk (Chapter 7). In sum, this dissertation links studies of mechanism with hypotheses about function in order to illuminate the evolutionary roots of human's unique cognitive phenotype.
Item Open Access What Makes Our Minds Human? Comparative Phylogenetic Perspectives on the Evolution of Cognition(2012) MacLean, EvanWhat makes our minds human? How did they evolve to be this way? This dissertation presents data from two complementary lines of research driven by these orienting questions. The first of these explores the `what' of human cognitive evolution through comparative studies with chimpanzees and bonobos. The general aim of these studies is to understand which aspects of cognition are unique to humans, and which are shared with our closest living relatives. Chapters 2-3 test the hypothesis that humans have unique cognitive skills for reasoning about the attention of other individuals (theory of mind), and unique motivation to use these skills in cooperative contexts with conspecifics. In Chapter 2 I show that understanding others' attention is unlikely to be the `small difference that makes the big difference', as some researchers have proposed. However, my data support the possibility that species differences in the ontogeny of these skills may have robust consequences for the adult cognitive phenotype. In Chapter 3 I show that (contrary to previous reports) nonhuman apes are also motivated to engage in some simple triadic social activities, which resemble those characteristic of human children. Again however, I identify important differences between humans and other apes in their spontaneous preferences for these types of activities, and their attitudes toward a partner when cooperative behaviors are interrupted. The second half of this dissertation (Chapters 4-5) explores the `why' and `how' of cognitive evolution. Chapter 4 outlines the kind of research questions and methods that comparative psychologists will need to embrace in order to use the comparative method to its full potential in the study of cognitive evolution. Chapter 5 provides a proof of principle for this approach using a dataset including 33 species tested on two cognitive tasks measuring inhibitory control. Here I show that cognitive skills for inhibitory control are closely related to phylogeny across species, and strongly predicted by absolute (but not relative) brain size. Further, I show that two of the other leading hypotheses put forth to explain primate intelligence, namely sociality and diet, do not predict cognitive skills on these tasks. These data illustrate the power of the comparative method for understanding cognitive evolution, and provide a starting point for future studies embracing this approach. Collectively, this research refines our understanding of how human cognition differs from that of other primates, and illustrates the utility of studying cognitive evolution from an explicitly phylogenetic comparative framework.
Item Open Access Why Does Risk-Taking Peak During Adolescence?: Contribution of Neurochemical and Circuit-Level Function to Lower Serotonin-Mediated Behavioral Inhibition in Adolescents(2012) Arrant, AndrewAdolescence is the period of transition between childhood and adulthood, and is characterized across mammalian species by changes in behavior that include increases in risk taking, novelty/sensation seeking, and social behavior. Immaturity of the central serotonergic system during adolescence could contribute to risk taking behavior by resulting in lower avoidance of aversive stimuli in adolescents than adults. The purpose of this dissertation was to investigate whether immature serotonergic function could contribute to adolescent risk taking. We studied pre- and postsynaptic serotonergic function and circuit-level mechanisms relevant to risk taking behavior using behavioral and neurochemical approaches.
Serotonergic modulation of behavior was assessed in adult (67-74 day old) and adolescent (28-34 day old) male rats in the novelty induced hypophagia (NIH), elevated plus maze, (EPM), and light/dark (LD) tests for anxiety-like behavior. Serotonin depletion with the synthesis inhibitor p-chlorophenylalanine (PCPA) produced anxiolytic effects only in adult rats in the NIH test and in both age groups in the EPM. These data showed that some serotonin-mediated behavioral inhibition is present during adolescence. However, adolescent rats were less sensitive than adults to the anxiogenic effects of the serotonin releasing drugs fenfluramine and methylenedioxymethamphetamine (MDMA) and the serotonin uptake inhibitor fluoxetine in the LD test, suggesting that serotonin is not as effective at inhibiting behavior in adolescents as it is in adults.
Microdialysis conducted in medial prefrontal cortex (mPFC) showed that adolescent rats exhibited lower increases in extracellular serotonin after treatment with the releasing drug fenfluramine, but not the uptake inhibitor fluoxetine. Further investigation of presynaptic serotonin function in adults and adolescents revealed that adolescent rats have lower tissue serotonin content than adults in several forebrain regions, but similar rates of serotonin synthesis, density of serotonin transporter (SERT)-immunoreactive innervation, and SERT radioligand binding. These data suggest that adolescents may have a lower increase in extracellular serotonin than adults after a releasing drug, but not an uptake inhibitor, due to lower tissue serotonin stores. Lower serotonin stores may limit the ability of a releasing drug to increase extracellular serotonin, but are unlikely to affect response to an uptake inhibitor. These findings also indicate that extracellular serotonin does not completely account for lower serotonin-mediated behavioral inhibition in adolescents.
Since presynaptic serotonin function did not explain age differences in the anxiogenic effects of indirect serotonin agonists, we investigated postsynaptic serotonin signaling by testing the behavioral effects of serotonin receptor agonists in the LD test. Adolescent rats were less sensitive than adults to the anxiogenic effects of the 5-HT1A agonist 8-hydroxy-2-(dipropylamino)tetralin (8-OH DPAT) in the LD test, but not to the 5-HT2 agonist meta-chlorophenylpiperazine (mCPP). No age differences were observed in 3H-8-OH DPAT binding in prefrontal cortex, amygdala, or hippocampus between adolescents and adults, and infusion of 8-OH DPAT into mPFC (prelimbic cortex), ventral hippocampus, or basolateral amygdala was unable to replicate the systemic effects of 8-OH DPAT. These data suggest that lower adolescent sensitivity to the anxiogenic effects of 8-OH DPAT is not due to age differences in receptor expression, and show that 5-HT1A stimulation in mPFC, ventral hippocampus, and basolateral amygdala alone is not sufficient to mimic the effects of systemic 8-OH DPAT.
We tested the circuit-level effects of fluoxetine and 8-OH DPAT, since stimulating 5-HT1A receptors in single brain regions failed to reproduce age differences in systemic 8-OH DPAT administration. Both drugs activated regions of the amygdala more in adults than adolescents, and 8-OH DPAT also produced greater prefrontal cortical activation in adults. Fluoxetine produced greater expression of the immediate early gene c-Fos in regions of the extended amygdala in adult rats, and 8-OH DPAT produced greater activation of the lateral orbital cortex and central amygdala in adult rats. Lower activation of cortical and amygdala brain regions could underlie the lower behavioral effects of these drugs in adolescents, as these brain regions are important in mediating behavioral inhibition and anxiety-like behavior. These data are also consistent with human studies showing immature cortical and amygdala function during adolescence.
This dissertation shows that adolescents are less sensitive than adults to serotonin mediated behavioral inhibition, and that this may be due to immature activation of neural circuits modulated by the 5-HT1A receptor between the prefrontal cortex and amygdala. This immature serotonin mediated behavioral inhibition could contribute to adolescent risk taking, drug abuse, and increased risk for suicidality during SSRI therapy for depression and mood disorders.