Biology Theses and Dissertations

Permanent URI for this collectionhttp://hdl.handle.net/1903/2749

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INTERACTIONS OF SOCIAL EXPERIENCE, ALCOHOL SENSITIVITY, AND THE SEROTONERGIC SYSTEM
(2024) Ho, Ta-wen; Herberholz, Jens; Neuroscience and Cognitive Science; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
Social isolation has been shown to correlate with increased alcohol consumption in various animal species. In humans, a decreased sensitivity to acute alcohol is correlated with future alcohol dependence and addiction. A plausible explanation for this correlation is that alcohol sensitivity decreases after isolation; however, our understanding of the mechanistic interaction between social isolation and sensitivity to acute alcohol is still in its infancy. The serotonergic system is one promising candidate that could be involved in this interaction because of its wide range of behavioral and physiological effects, especially those related to social experiences. In my dissertation, I investigated the roles of the serotonergic (5-HT) system with three separate aims: In the first aim, I measured the effects of several 5-HT agents (neurotoxin, reuptake blocker, and receptor agonist/antagonists) in freely-behaving crayfish that were communally housed (COMs) or individually isolated (ISOs) prior to ethanol (EtOH) exposure. I found that 5-HT is important in regulating the social differences in EtOH sensitivity, and 5-HT2βPRO receptors emerged as candidates to produce this interaction between 5-HT and EtOH. My results from this aim suggest that these receptors are downregulated in isolated crayfish, leading to reduced behavioral EtOH sensitivity. The second aim employed single-cell neurophysiology and pharmacology in the lateral giant (LG) circuit of reduced ex vivo crayfish preparations to investigate the cellular-molecular mechanisms that underlie the interaction between 5-HT and specific EtOH receptor targets. I found that the LG neurons are stimulated by EtOH, and social differences in EtOH sensitivity between COMs and ISOs are paralleled at the level of these single neurons. Specifically, my results suggest that social isolation causes downregulation of 5-HT2βPRO receptors and 5-HT1αPRO receptors on the LG neurons and upregulation of these receptors subtypes in GABAergic neurons that send feed-forward inhibition onto the LG neurons. In my third aim, I developed a wearable, miniature, cyclic voltammetry device that is capable of detecting (injected) monoamine neurotransmitters (including 5-HT) in freely-behaving crayfish. With improved sensor sensitivity in the future, this will allow measurements of 5-HT release patterns in crayfish with different social histories, including during EtOH exposure. Together, the results from my dissertation will inform work in other model systems and improve our understanding of the interactions between social experience, the 5-HT system, and alcohol use.
Sculpting Sounds: INTRINSIC PHYSIOLOGY AND INHIBITORY ANATOMY OF THE AVIAN AUDITORY BRAINSTEM
(2024) Baldassano, James; MacLeod, Katrina; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
Soundwaves are rapidly modulated, multi-dimensional stimuli. The cochlea decomposes these signals into frequency and intensity information which is conveyed via the auditory nerve into the brain. How does the brain manage to extract these multidimensional signals from auditory nerve activity? How does it sculpt this input so that both the microsecond precision of “where?” and the spectrotemporal modulations of “what?” are encoded with high fidelity? Birds are powerful models for studying early auditory processing because they interact with sounds similarly to mammals but have a simpler neuronal architecture. We describe the intrinsic physiology and anatomy and auditory brainstem neurons involved in spectrotemporal processing. In birds, the auditory nerve synapses onto two anatomically distinct cochlear nuclei, cochlear nucleus magnocellularis (NM) which encodes frequency/timing information, and the more heterogeneous cochlear nucleus angularis (NA) which encodes intensity information. NA has been shown to encode the acoustic envelope, likely through a subset of neurons that respond preferentially to modulations in their inputs via an adaptive spike threshold. We first examined the intrinsic basis of this adaptive threshold and found that a dendrotoxin-sensitive low threshold potassium conductance is responsible for it. In addition to the intrinsic properties of neurons, inhibition sculpts a number of auditory processes. The majority of inhibition in the avian auditory brainstem originates in the superior olivary nucleus (SON), which has multiple response types & projects either to multiple lower order ipsilateral nuclei, including NA & NM, or to the contralateral SON. Retrograde labeling experiments have demonstrated that these projections originate from distinct populations of SON neurons, however it is not clear if there is a relationship between response types and postsynaptic target. We used in vitro electrophysiology and neuronal reconstruction to establish a relationship between response types and targets. While the function of inhibition is well documented in timing circuits, its role in intensity processing is less clear. We used dynamic clamp to model inhibitory conductances while recording from NA neurons in vitro to determine how inhibition impacts the range of inputs that a NA neuron can encode before its firing rate saturates.
Sex and the Evolution of a Double Hermaphrodite
(2023) Ficklin, John Alexander; Haag, Eric S; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
The Kryptolebias marmoratus species complex contains the only known self-fertile hermaphroditic vertebrates. There are three species in this clade and all three live in the mangrove forests across the tropical Americas. All three have individuals with both testis and ovarian tissue in their gonads with two using self-fertility as their main mode of reproduction, and all three have apparent different sex determination and sexual modes. In this dissertation, I explore aspects of sex in these species. K. marmoratus is the androdiecious and self-fertile member of the species complex with sequential hermaphroditism. In this species, the control of sex change from hermaphrodite to male is poorly understood. Individuals that were believed to be genetically identical could be raised in the same environment and change sex at drastically different times or not at all. Small fluctuations and variance in the hormonal profiles of individuals was thought to be a potential cause and while androgen dosing can lead to masculinization of both the gonad and the soma, it was not enough to maintain a permanent transition like what is seen in nature. In K. ocellatus, the obligate outcrosser of the K. marmoratus species complex, it was believed that they were using genetic sex determination to differentiate between males and the females that had hermaphroditic gonads. While we found strong evidence against heteromorphic sex chromosomes, all tests for homomorphic sex chromosomes came back inconclusive due to apparent K. hermaphroditus DNA contaminating the dataset. K. hermaphroditus, the self-fertile hermaphrodite species with exceptionally rare males, appears to be extending its range further and further south and/or hybridizing with K. ocellatus at rates previously underappreciated. The hermaphrodites of the Kryptolebias genus still hold many evolutionary and physiological secrets but can potentially be revolutionary to the understanding of vertebrate sexual development and evolution.
DIVERGENT MATING STRATEGIES ACROSS THE PEROMYSCUS GENUS DRIVE REPRODUCTIVE TRAIT DIVERSITY
(2022) Weber, William David; Fisher, Heidi S; Behavior, Ecology, Evolution and Systematics; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
The study of sexual selection and reproductive biology are dynamic research fields that contribute to basic research, public health, agriculture, and conservation. Peromyscus mice are an important model for studying the evolution of reproductive traits shaped by sexual selection due to the natural diversity of mating systems in this genus. Like most rodents, the ancestral mating strategy of Peromyscus is believed to be promiscuity, but monogamy has evolved independently at least twice. In this dissertation, I investigate how the divergent mating systems in Peromyscus have shaped the diversity of reproductive traits using six species (three monogamous and three promiscuous). First, I characterize the estrous cycle and show that promiscuous species display more intense estrous signaling than monogamous species, but I find a uniform cycle length across the genus. Moreover, I report a method to hormonally-induce ovulation in two species, P. polionotus (monogamous) and P. maniculatus (promiscuous). Second, to investigate the co-evolution of male and female reproductive traits, I examined six species that have evolved under divergent sexual selection pressures and found a correlated expression of traits associated with sperm competition in males and control of fertilization in females. Third, I focus again on P. polionotus and P. maniculatus to examine how mating system influences male response to perceived competition for reproductive success using resident-intruder introductions. I found that while the males of monogamous species were highly aggressive toward rivals, the promiscuous species increased sperm production, which is predicted to increase fertilization success when females mate multiply. Together, this research both characterizes and functionally tests how evolutionary history and social interactions have shaped the diversity in reproductive traits of Peromyscus mice.
PHYSIOLOGICAL CHARACTERIZATION OF SPECIFIC LOCAL INTERNEURON SUBPOPULATIONS IN THE DROSOPHILA ANTENNAL LOBE
(2022) Schenk, Jonathan Edward; Gaudry, Quentin; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
The olfactory system of the fruit fly Drosophila melanogaster is an invaluable model for understanding circuit function. Composed mainly of olfactory receptor neurons (ORNs), projection neurons (PNs), and local interneurons (LNs), it is an analogous structure to mammalian olfactory systems. Of these cell types, LNs are particularly intriguing. These neurons are found in a variety of morphologies and with differing neurotransmitter and receptor profiles. Given their heterogeneity, it is critical to gain an understanding of their roles in olfactory circuits. In this work, I probe the physiology and functions of two unique subpopulations of LNs in the antennal lobe (AL). In the first population, I demonstrate LNs which respond to extrasynaptic, paracrine levels of serotonergic modulation. These LNs then engage in postsynaptic inhibition and subtractive gain control, which is contrary to typical LNs. The second population I characterize are previously undescribed nonspiking LNs in the fly AL. Nonspiking cells are common to insect olfaction as well as other sensory pathways in vertebrates. I find that these neurons are likely to be electrotonically compartmentalized, such that activation within individual regions does not propagate across the whole cell, suggesting roles in previously unexplained mechanisms such as intraglomerular inhibition. The results of this work suggest more heterogeneity in Drosophila LNs than previously assumed and cements the importance of interneuron contribution to neuronal function.
Physiological dynamics of injury and regeneration in the clonal freshwater annelid Pristina leidyi
(2022) Rennolds, Corey William; Bely, Alexandra E; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
The threat that mechanical injury poses to homeostasis and survival has spurred the evolution of diverse processes to mitigate these effects. The most dramatic of these is regeneration, a process that restores the form and function of lost body parts. The apparent benefits of regeneration may come at considerable cost, however, and these may substantially diminish regeneration’s adaptive value in certain contexts, potentially contributing to evolutionary losses of regeneration. The costs and benefits of regeneration are poorly understood in most animals, precluding more than speculation of the evolutionary drivers of regeneration. Naids are a group of small, clonally reproducing freshwater annelids that feature great diversity of regenerative ability and are well suited to experimental studies. I used the species Pristina leidyi to determine how injury and regeneration affect organismal function and fitness, integrating physiological and molecular approaches. I first investigated how injury and regeneration differentially affect an individual’s ability to tolerate environmental stress, an ecologically relevant and energetically demanding task. I found that stress tolerance is reduced by regeneration in a stressor- and tissue-specific manner while, unexpectedly, tolerance is temporarily improved shortly after injury. These effects are unrelated to whole-organism metabolic rate, which surprisingly does not differ between early and late injury recovery. Using 3’ TagSeq, I found that, while injury and heat stress elicit largely distinct responses, both upregulate certain shared damage control pathways. I then tested whether the physiological cost of regeneration has potential to translate into fitness costs by examining the interaction between regeneration and reproduction, which occurs by asexual fission in this species. By modulating resource availability, I found evidence for an energetic trade-off between regeneration and reproduction that is masked when food is abundant. This tradeoff is manifested through a reduction in per-offspring allocation rather than reproductive rate. Overall, my results demonstrate that injury and regeneration costs are highly context dependent in P. leidyi. More broadly, these findings contrast in key ways from evolutionarily distant animals with very different life history traits, illustrating the importance of investigating the physiological mechanisms that may mediate selection on regeneration in diverse lineages.
EXAMINING THE GENETIC BASIS AND PHYSIOLOGY OF SURVIVAL IN EXTREME LOW SALINITY TO IMPROVE AQUACULTURE OF THE EASTERN OYSTER Crassostrea virginica
(2022) McCarty, Alexandra J; Plough, Louis; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
The eastern oyster, Crassostrea virginica, is an important aquaculture species and supports a growing industry along the east coast of the United States. However, increases in freshwater from storm events and intentional diversions can expose coastal aquaculture operations to extreme low salinity (< 5), resulting in reduced productivity and mortality. The primary objectives of this dissertation were to investigate the biology and genetic basis of low salinity tolerance to improve eastern oyster aquaculture. In Chapter 2, I developed and conducted a series of extreme low salinity (2.5) challenges to estimate the quantitative genetic parameters of low salinity survival. A moderate narrow-sense heritability was estimated for challenge survival, h2 ≈ 0.4. In addition, osmolality of hemolymph collected from oysters during the first week of the challenge suggest that all individuals conformed to the surrounding low salinity regardless of challenge survival. In Chapter 3, I performed additional low salinity challenges to assess the importance of challenge duration (2 or 6 months) and temperature (chronic or fluctuating) on low salinity survival. I also investigated algae removal during the chronic challenge to better understand oyster response during low salinity stress. Phenotypic (rS = 0.89) and genetic (rG = 0.81) correlations between family mortality were high across the two challenges, indicating that a 30-day exposure at a constant low salinity (2.5) and temperature (27°C) is a sufficient progeny test for low salinity survival. Modest associations between algae removal metrics and survival in extreme low salinity indicate that individual feeding ability may relate to differential low salinity survival. Lastly, in Chapter 4, I performed genome mapping to investigate the genomic architecture of low salinity survival. Quantitative trait locus mapping and linkage disequilibrium analysis revealed a significant region on eastern oyster chromosome 1 and 7. Genomic prediction accuracies for survival and day to death in extreme low salinity were moderate and encouraging, 0.49 – 0.57. The results from my dissertation characterize the genetic basis of survival during low salinity events and support the incorporation of this trait into breeding efforts to improve production and enhance the resiliency of the eastern oyster aquaculture industry.
PHYSIOLOGICAL, MOLECULAR, AND ECOLOGICAL RESPONSES OF THE EASTERN OYSTER, CRASSOSTREA VIRGINICA, TO HYPOXIA EXPOSURE IN THE CHESAPEAKE BAY
(2021) Davis, Anna Manyak; Plough, Louis; Marine-Estuarine-Environmental Sciences; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
Hypoxia is a naturally occurring phenomenon in coastal waters that is increasing in frequency and extent due to human activities. There is a pressing need to understand how organisms will be able to respond and adapt to future oxygen limitation. The eastern oyster, Crassostrea virginica, is an ecologically important bivalve that is threatened by the increasing incidence of low oxygen events. Little is known about the capacity of C. virginica to cope with projected deoxygenation or the potential ecological implications of reduced oxygen availability. The primary objectives of this dissertation research were to 1) characterize the intraspecific variability in physiological and molecular responses to hypoxia for oysters from the Chesapeake Bay and 2) develop a model to predict the implications of hypoxia on oyster population ecology. In Chapter 2 I assessed the survival and heart rate responses under low oxygen stress for oysters sourced from reefs experiencing varying frequencies of hypoxia exposure. Results indicated that prior hypoxia exposure does not confer increased survival under low oxygen stress but may relate to sublethal physiological differences in tolerance, particularly for oysters with a greater frequency of prior hypoxia exposure. In Chapter 3, I used four different analytical approaches, principal components, differential gene expression, co-expression gene network, and transcriptional frontloading analyses, to assess intraspecific differences in oyster transcriptomic response to hypoxia. No statistically significant differences in gene expression response between sites were observed indicating that prior hypoxia exposure may not have affected the regulation of expression under hypoxic stress. However, while not statistically significant, gene expression patterns suggested transcriptional frontloading as a possible mechanism of increased hypoxia tolerance in oysters. Finally, in Chapter 4, I developed a Dynamic Energy Budget model integrating dissolved oxygen concentration as a forcing variable to make predictions about oyster growth and reproduction under varying oxygen conditions. Model outputs indicated that low oxygen exposure reduces oyster growth, fecundity, and spawning frequency. Collectively, this dissertation research affirms that low oxygen availability negatively affects oyster physiology and ecology, and emphasizes the importance of continued research into the capacity of oysters to tolerate future increases in coastal hypoxia.
Extratympanic hearing in salamanders: A comparative assessment of structural variation and terrestrial function of an atympanic ear
(2021) Capshaw, Grace; Carr, Catherine E; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
The auditory system mediates the detection of acoustic cues and enhances survival within complex environments by enabling organisms to construct an auditory scene of their surroundings. The tympanic middle ear evolved multiple times in all terrestrial tetrapod lineages to overcome the impedance mismatch encountered by sound pressure at the air-skin boundary, indicating its significance for aerial hearing; however, fossil evidence demonstrates that the earliest terrestrial tetrapods retained aquatically-adapted ears that were unspecialized for detecting airborne sound. How did these unspecialized ears function on land? Comparative study of extant atympanate vertebrates can provide key insights into the ancestral state and early evolution of the terrestrial tetrapod auditory system following the water-to-land transition. In this dissertation, I use atympanate salamanders as a model to investigate the structural and functional parameters underlying terrestrial hearing with unspecialized ears. In chapter one, I review the biology of the salamander auditory system. In chapter two, I characterized morphological variation of the salamander ear and found evidence for habitat-related specialization, suggesting underlying physiological variation. In chapter three, I measured auditory sensitivity to sound pressure and seismic vibration, and observed variation in sensitivity that corroborates the ecomorphological trends reported in chapter two. I assessed the contributions of hypothesized extratympanic pathways for hearing, including seismic sensitivity, cavity resonance, and bone conduction. I determined that aerial auditory sensitivity is mediated by bone conduction of sound as head vibrations that are detectable to the inner ear. In chapter four, I evaluated the sound localization capabilities of an atympanic ear. I found that bone conduction hearing in salamanders supports a figure-eight pattern of directional sensitivity to airborne sound. I contextualize my findings with other studies of tympanate and atympanate taxa and suggest that bone conduction may represent a general mechanism enabling aerial sound detection and localization in terrestrial species with atympanic ears.
MOLECULAR EVOLUTION AND BIOPHYSICAL CHARACTERIZATION OF PLANT GLUTAMATE RECEPTOR-LIKE ION CHANNELS
(2020) Simon, Alexander; Feijό, José A; Biology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)
Plant and animal cells live in different ionic milieus and evolved different electrical membrane properties. As membrane transport in plants and animals has diversified through the population of ion channels to tailor signaling strategies, the glutamate receptor superfamily has emerged to conserve a prominent role in Ca2+ and electrical signaling. Ionotropic glutamate receptors (iGluRs) in the mammalian central nervous system are ligand-gated cation channels. Their specificity for glutamate as a ligand required to promote ion channel opening is critical to fast excitatory synaptic transmission and is indispensable for higher cognitive function. Plant glutamate receptor-like channels (GLRs) are also involved in Ca2+ and electrical signaling for a breadth of biotic and abiotic stress responses, sexual reproduction, and cell-cell communication events as determined by genetic analysis. However, the biophysical underpinnings to GLR’s role in cell signaling have only begun to emerge. We addressed the evolutionary conservations of function within the glutamate receptor superfamily and their specialization for plant membrane transport by means of genetics and an electrophysiological characterization of GLR1 encoded by the moss Physcomitrium patens (PpGLR1) using whole-cell patch clamp and Ca2+ imaging. We present a role of PpGLR1 in moss development as a homomeric ion channel involved in light signal transduction that suggests a conservation of function with GLRs found in angiosperms at the physiological level. At the molecular level, we identify the extracellular ligand binding domain of plant GLRs retains structural homology to iGluRs—without the glutamate specificity— while CORNICHON homolog proteins (CNIHs) also have a conserved role in glutamate receptor gating. We further establish distinctive properties of GLRs in ion channel gating and ion selectivity derive from the transmembrane channel pore. The pore works as a direct gate and co-opts the ion selectivity necessary for a membrane depolarization in plant cells by yielding a strong anion permeability with weak mono-cation and Ca2+ permeability. By targeted-mutagenesis, the PpGLR1 selectivity filter was swapped out for the mammalian GluA2 (Q-form) selectivity filter converting a predominantly anion-selective channel poorly responsive to ligands into a primarily cationic channel significantly potentiated by the ligand ACC (1-aminocyclopropane-1-carboxylic acid). These results map the molecular evolution of glutamate receptors shaping the ion channel properties conserving plant GLR’s role in Ca2+ and electrical signaling.

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