Entomology
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Item EXAMINING INTERACTIONS AMONG FUNGAL INFECTION, SLEEP, AND HOST DEFENSE IN POPULATIONS OF WORLDWIDE, SLEEP INBRED PANEL, AND MUTANT DROSOPHILA MELANOGASTER(2024) Nan, Mintong; St. Leger, Raymond; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Previous studies with mutant Drosophila melanogaster lines and the Drosophila Genetic Reference Panel (DGRP) reveal substantial variation in susceptibility to infection with Metarhizium anisopliae strain Ma549. These differences likely arise from variations in immunity, physiology, and behavior, yet the role of selection pressures in maintaining these disparities remains understudied. Using global Drosophila populations, the Sleep Inbred Panel (SIP), and sleep-deprived mutants, we investigated the interactions among fungal infection, sleep, and host defense. Testing 14,957 male and 15,287 female flies from 43 lines across 28 locations, we found that resistance to Ma549 correlates with latitudinal gradients in sleep duration, temperature, and humidity. Tropical populations may exhibit stronger defenses due to fungal diversity; however, the most disease-resistant males were also more susceptible to desiccation, indicating trade-offs between abiotic stress and disease resistance. Longer-sleeping males and virgin flies survived infections longer, and increased daytime sleep post-infection was particularly protective in resistant flies. These findings suggest that sleep and disease resistance are interrelated traits possibly shaped by clinal evolution. Using 10,917 males and 11,166 females selected for extreme long or short nighttime sleep duration, we found that short-sleepers, despite having fragmented sleep when healthy, outlived long-sleepers after Ma549 infection. Resistance differences were sex-specific: males were more resistant among short-sleepers, while females showed higher resistance among long-sleepers. Daytime sleep bout numbers correlated with dimorphic disease resistance. Additionally, Ma549 infection increased daytime sleep in both short- and long-sleepers, with short-sleeping males nearly matching long-sleepers in sleep duration post-infection. Virgins, regardless of sleep status, slept more and survived infection longer, indicating that sleep traits, sex, and mating status are closely linked to disease resistance. The study highlights that circadian rhythms influence sleep and immunity, with the sleep-deprived Shmns mutant failing to undergo sickness sleep and succumbing quickly to infection. Mutants with disrupted circadian rhythms (PER and CLK) also showed impaired sickness sleep; however, only the per gene offered protection against disease, while the Clk mutant had increased survival. Independent of mutant status, males slept more than females, and virgins slept more than mated flies, emphasizing the significance of circadian rhythms in sleep and disease resistance.Item Elucidating factors to improve biological control of Halyomorpha halys by egg parasitoids(2023) Potter, Madeline Elizabeth; Shrewsbury, Paula M; Burghardt, Karin T; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Halyomorpha halys Stål (Hemiptera: Pentatomidae), also known as the brown marmorated stink bug, is an invasive species from Northeast Asia, which has now spread to 47 USA states and invaded several other countries. In the USA, H. halys is an economically important pest of fruit, vegetable, field, and nut crops, and it feeds on ornamental plants. A sustainable means of controlling this pest is needed. Here I focus on elucidating features from bottom-up forces (alternate host identity, host plant identity, and habitat type) which may influence top-down forces such as parasitism by H. haly’s key natural enemies, Hymenoptera egg parasitoids. Naturally laid eggs of insects were collected from a tree nursery in 2020 and from diverse habitats throughout Maryland in 2021 to investigate H. halys parasitoids’ alternate insect egg hosts, host plant and habitat associations, and which factor(s) (host plant identity and/or host egg identity) are important to egg mass discovery, or to egg parasitism rate. Effects of host insect feeding guild (herbivore vs predator) and host plant origin (native vs non-native) on parasitism were also examined. One new overwintering insect host and four new in season hosts for Anastatus spp., and five new in season hosts for Telenomus cristatus were found. A diverse array of plant species, particularly native Acer and Quercus species, were found to support alternate host insects. Halyomorpha halys related parasitoids were reared from eggs collected in all habitat types. Host egg order and egg feeding guild affected Anastatus spp. egg unit discovery efficiency and egg parasitism rate. Host plant identity and plant origin affected egg unit discovery efficiency and egg parasitism rate by all H. halys parasitoids. These findings support the importance of having a diverse community of alternate prey and informed plant selections to support parasitoids and their biological control of H. halys and other insect pests.Item Urbanization and Landscape Heterogeneity Influence Culex Species Ecology and Genetics in Eastern North America(2023) Arsenault-Benoit, Arielle L.; Fritz, Megan L.; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Vector-borne disease is an important facet of public health, as they account for nearly 20% of global disease burden. Multiple species, including at least one vector, at least one host, and a pathogen, must interact in vector-borne disease transmission cycles, and thus understanding human risk of vector-borne disease and public health outcomes requires a community ecology framework. Members of the Culex genus, including Cx. pipiens, Cx. quinquefasciatus, and Cx. restuans are sympatric in eastern North America and are vectors of West Nile virus. This dissertation explores the roles of habitat use, community ecology, phenology, and landscape heterogeneity on Culex spatiotemporal dynamics and genetics along urban to rural gradients in eastern North America. Through surveillance of belowground structures in Washington, D.C. over two years, I found that mosquito species of public health importance, including Aedes aegypti, Aedes albopictus, and members of the Culex pipiens assemblage, use these structures for breeding and development. Belowground structures may serve as refugia against extreme climatic conditions and facilitate overwintering survival for non-diapausing taxa and/or taxa with thermal tolerance limitations, potentially expanding their suitable ranges. On an urban to rural gradient in greater Washington, D.C. and Maryland, a complex of cryptic Culex WNv vectors co-occur on the landscape. Using molecular techniques and constrained ordination, I found that these cryptic Culex species were differently distributed at fine spatial scales, likely due to the impacts of urbanization on vector habitat and subsequent niche segregation. Culex pipiens were cosmopolitan and dominant across sites in greater Washington D.C. and Maryland. However, individuals with Cx. quinquefasciatus ancestry were limited to urban and peri-urban sites closest to the city center, and Cx. restuans were most abundant in rural and suburban sites furthest from the city center with dense and heterogeneous canopy cover. Previous work suggested that phenology has a considerable impact on Culex species dynamics; Cx. restuans was thought to be an early season species that cedes to Cx. pipiens over the course of the season. Initially, I did not detect an effect of season on Culex spatiotemporal dynamics when collections were undertaken from June through October, but when I expanded the collection season to include the months of April and May, the influence of season was evident. Therefore, the hallmark “crossing-over” point that is common in the Culex literature happens prior to the local mosquito abatement season in Washington and D.C. and Maryland. During the active surveillance and management period, season has little impact on Culex species abundance as compared to environmental factors measured along our urban to rural gradient. A replicated comparison of the abundance and relative frequency of Cx. pipiens and Cx. restuans along urbanization gradients in Washington D.C., greater Philadelphia, PA and greater Chicago, IL, using gradient forests demonstrated that phenology was consistently the most important predictor of the shift between a Cx. restuans-dominant community and a Cx. pipiens-dominant community. This crossing-over point trended later in the season with increasing latitude. Turnover in species abundance tended to occur at intermediate points along environmental gradients associated with urbanization, like percent impervious surface, percent tree cover, distance to city center, and vegetation index. Results of two analytical approaches (ordination and regression trees) and from three metropolitan areas support Cx. restuans as an early season species that is otherwise associated with sites with cooler temperatures, less impervious surface, more tree cover, a shallower water table, and increased distance from city center. Conversely, Cx. pipiens is more abundant than Cx. restuans in sites that are more characteristic of urbanization. Culex pipiens is globally ubiquitous and was common across site classes in the three localities in this study. This species comprises two bioforms, pipiens and molestus, which are characterized by divergent ecological, physiological, and behavioral traits. These bioforms can interbreed in the field and the lab. However, at all sites analyzed across three northeastern metropolitan areas, analysis of genotypes at a single neutral locus violated assumptions of Hardy Weinberg Equilibrium, suggesting that there is not unrestricted geneflow between bioforms across the landscape. The proportion of molestus alleles increased with increasing percent impervious surface and decreased vegetation, two environmental correlates of urbanization. Molestus alleles may confer an advantage in urban environments because they can leverage human infrastructure to overcome thermal limitations and persist in isolated belowground populations via autogeny and use of mammalian hosts. Overall, Culex WNv vectors are differentially distributed across urban to rural gradients in the northeastern United States. These aspects are influenced by a heterogeneous land use and landscape-level changes associated with urbanization. A clear understanding of vector life history, genetics, interspecies interactions, and distribution across the landscape can improve practitioners’ power and precision in predicting and managing vector borne disease transmission. While some patterns in species distribution and composition were universal across metropolitan areas, there was variation between localities that could significantly contribute to WNv transmission and human disease risk. Therefore, I conclude that modeling, as well as development of surveillance and management strategies for WNv vectors should be implemented locally to have the greatest impact on public health outcomes.Item Quantifying the relative contribution and furthering qualitative understanding of ftz cis-regulatory elements in Drosophila melanogaster(2022) Fischer, Matthew Douglas; Pick, Leslie; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Embryonic development is coordinated by interactions within gene regulatory networks. This process is orchestrated at the level of transcription through the regulatory properties of enhancers, which direct spatiotemporal expression patterns when bound by specific trans-acting factors. Though enhancers can act upon promoters located at great distances irrespective of orientation, the contributions from these cis-regulatory elements (CREs) are limited by insulators and/or tethering elements that organize chromatin architecture. Much research has been conducted towards understanding the coordination of the segmentation genes that pattern the basic body plan of the fruit fly, Drosophila melanogaster, during embryogenesis. The pair-rule genes (PRGs) of this pathway, such as fushi tarazu (ftz), are expressed in seven alternating stripes across the embryo. These PRGs are required for the development of body segments, and the mis-regulation of a single transcriptional domain can result in the loss of a segment. Here, I have investigated the ftz CREs to more precisely determine their sufficiency to direct expression within ftz stripe domains and their necessity for doing so in the native context of the gene. To investigate the sufficiency, I have generated 36 standardized reporter transgenes from 18 CREs, tested in both forward and reverse orientations. All CREs examined have been inserted into the same XbaI site of the reporter plasmid, and the transgenes have been inserted into the same genomic region. Through in situ hybridization experiments, I have determined that the qualitative patterns conferred by every CRE is orientation-dependent, and I have identified two putative insulators and/or tethering elements, proposed to explain this observation. To investigate their necessity, I targeted four genomic regulatory regions for precise deletion using the CRISPR/Cas9 system to generate seven deletion mutants. Though deletions were expected to cause lethality, most of the mutants are homozygous viable and fertile; only a mutant simultaneously removing two seven-stripe CREs was homozygous lethal. Quantitative gene expression analysis by fluorescent in situ hybridization chain reaction revealed that there is a critical threshold of ftz abundance required in each stripe for segmentation to proceed. In conclusion, I have determined that the ftz CREs are redundant and function together in a non-additive manner.Item COMBINING THE DROSOPHILA AND METARHIZIUM MODEL SYSTEMS TO INVESTIGATE HOST-PATHOGEN INTERACTIONS(2021) Wang, Jonathan; St. Leger, Raymond; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Even closely related individuals vary in their response to infection. In this dissertation, I combined the fruit fly model system with multiple pathogens, including 16 strains of the fungus Metarhizium, to dissect how pathogens with different virulence strategies interact with variable host resistance and tolerance mechanisms. I began by infecting 188 sequenced Drosophila melanogaster lines [the Genetic Reference Panel (DGRP)] with broad host range Metarhizium anisopliae (Ma549) or the bacterium Pseudomonas aeruginosa (Pa14, originally from a human host). Resistance to the two pathogens was correlated (suggestive of general multipurpose defense mechanisms) and associated with oxidative stress sensitivity, starvation resistance, and in particular sleep indices (flies that take a lot of naps are particularly resistant to disease). I followed up by showing that this nonspecific defense extends to the specialist co-evolved Drosophila pathogen, Entomophthora muscae. A genome wide association study implicated several metabolic pathways and physiological processes in individual variation to disease, but not the canonical antifungal Toll immune pathway.Indeed, Metarhizium strains that killed faster induced a stronger and earlier Toll immune response, indicating virulence does not depend on suppressing immunity. Disrupting the Toll pathway component Dif only increased susceptibility to the early diverged broad host range Metarhizium frigidum, whereas flies disrupted in Persephone (a sensor of pathogen proteases) succumbed quickly to all Metarhizium strains. Microarray analysis of mutants revealed a suppressed transcriptomic response to infection when either Persephone or Dif were disrupted, with overlap with GWAS-implicated pathways.Item Diversity and structure of Metrosideros polymorpha canopy arthropod communities across space and time(2019) Tielens, Elske Karolien; Gruner, Daniel S; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Global biodiversity is under pressure from climate change, habitat fragmentation and other anthropogenic change, and our ability to predict biodiversity responses to change requires a better understanding of the processes that drive diversity and structure local communities. However, quantifying these processes has proven to be challenging for multiple reasons; diversity is multidimensional, and both diversity and the processes that generate it vary across scale. In this dissertation, I examine temporal and spatial patterns in community structure to test hypotheses about the drivers of local diversity and composition in communities of varying age, focusing on arthropod communities associated with the native tree Metrosideros polymorpha on the Hawaiian Islands. Analysis of Hemiptera (true bug) communities reveals a temporal pattern in community structure, where young substrate communities were variable in species composition and beta dispersion decreased with substrate age, indicating convergence. However, substrate age did not correlate with community dissimilarity in a directional way. Similarly, geographic distance did not correlate with compositional dissimilarity, suggesting a lack of dispersal limitation. I confirmed this result by examining connections between arthropod communities in a historically fragmented ‘kīpuka’ landscape, using species-area relationships and graph theory analyses. Finally, if canopy arthropods are dispersive and differences in species composition across sites are not driven by substrate age, local habitat characteristics may influence species composition. I determined the role of local beta diversity and identified habitat characteristics regarding forest structure and host leaf traits that are strong drivers of beta diversity and species composition. Then, to further explore local habitat drivers I examined forests with high intraspecific variation in co-occurring Metrosideros. In this hybrid zone, insect life history traits shape species’ response to intraspecific variation in host plant characteristics, highlighting the importance of including dimensions of biodiversity beyond taxonomic diversity. Together, these results demonstrate the importance of local habitat conditions for canopy arthropods, suggest that canopy arthropod communities are highly connected and that substrate age plays a limited role in determining local arthropod communities. Such insights into biodiversity and plant-insect interactions across temporal and spatial scale are integral to understanding and conserving our natural world.Item EVALUATING THE EFFECT OF POTATO LEAFHOPPER (EMPOASCA FABAE) FEEDING ON BIOLOGICAL NITROGEN FIXATION IN ALFALFA (MEDICAGO SATIVA)(2019) Thompson, Morgan; Lamp, William O; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Aboveground feeding by potato leafhopper (PLH), Empoasca fabae, (Hemiptera: Cicadellidae) causes significant injury to alfalfa (Medicago sativa), including disrupting translocation of fixed carbon from leaves to roots. Basal transport of fixed carbon in alfalfa fuels a critical mutualism between roots and nitrogen-fixing bacteria (Sinorhizobium meliloti). Above- and belowground nutrient allocation in alfalfa determines perennial persistence across growing seasons, as well as forage quality. Whether leafhopper feeding alters nutrient allocation and subsequently affects nitrogen fixation, however, is not clear. To test this, my objectives were 1) to examine the effect of different management strategies on PLH injury and nitrogen fixation, and 2) to quantify the amount and location of fixed nitrogen in whole alfalfa plants when fed on by leafhoppers. Overall, my work contributes to an understanding of how aboveground pest pressure can disrupt belowground processes in plants and ultimately affect the economic viability of crops for growers.Item POLLEN NUTRITION, PESTICIDES, AND PATHOGENS: INTERACTIVE EFFECTS ON HONEY BEE HEALTH(2017) Garavito, Andrew; vanEngelsdorp, Dennis; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)While a variety of stressors influence honey bee (Apis mellifera) health, it is the additive and interactive effects of these factors on bee health that have been driving modern research. We devised a set of two experiments to test the effects of multiple stressors on honey bee health. First, we grew sunflowers to test the effects of drought stress and seed treatment on sunflower pollen. We fed the pollen collected from these sunflowers to cohorts of bees that were either infected or uninfected with the microsporidian pathogen Nosema ceranae to find that drought stressed pollen leads to increased mortality in infected bees. Next, we fed 37 experimental pollen diets of different floral varieties and pesticide loads to honey bees infected with N. ceranae, but we were unable to find a connection between diet variety and pesticide exposure on bee health.Item Taxonomic revision, phylogenomic analyses, and natural history of the fungus-farming ant genus Sericomyrmex (Hymenoptera: Formicidae)(2016) Jesovnik, Ana; Mitter, Charles; Schultz, Ted R; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)Fungus-farming ("attine") ants, a New World clade of nearly 300 species in 16 genera, are model systems for studies of symbiosis, coevolution, and advanced eusociality. All attine ants cultivate fungal symbionts for food. "Lower" attine ants cultivate facultatively symbiotic fungi, but in "higher" attine ants both ants and fungi are obligate, highly coevolved symbionts. Sericomyrmex is a poorly studied higher-attine genus known for its problematic taxonomy. This work represents the first comprehensive study of Sericomyrmex species and their fungal cultivars. For Chapter One I sequenced, assembled, and analyzed transcriptomes of three species of Sericomyrmex and a lower-attine-ant species, Apterostigma megacephala. I characterize the transcriptomes, conduct phylogenetic analyses, and search for genes of interest, most importantly arginine biosynthesis pathway genes, the absence of which in A. megacephala strongly suggests that attine ants became dependent on their fungi early in their evolution. In Chapter Two I address the phylogenomics of Sericomyrmex, sequencing ~990 ultra-conserved-element loci for 88 Sericomyrmex samples. Maximum-likelihood and species-tree phylogenetic methods recover nearly identical topologies across data sets, identifying nine species-level lineages. Divergence-dating analyses indicate that Sericomyrmex is the product of a recent, rapid radiation, with a crown-group age estimate of 4.3 million years. I sequence two nuclear ribosomal regions for 32 Sericomyrmex fungi. The fungal phylogeny indicates that Sericomyrmex cultivars are generalized higher-attine cultivars, which, rather than forming a separate clade, are interspersed with Trachymyrmex-associated fungi, indicating cultivar sharing and horizontal transfer between those genera. In Chapter Three, guided by my phylogenomic results, I study the morphology of Sericomyrmex workers, males, queens, and larvae and conduct a comprehensive taxonomic revision, including a key to the worker caste and species distribution maps. Sericomyrmex comprises 11 species, including three new species. The number of recognized species is lower than the previously recognized 19 species and three subspecies. In Chapter Four I review the literature of and report newly acquired data on the natural history of Sericomyrmex, with a focus on nesting biology, presenting data for 19 nests of seven Sericomyrmex species.Item The alarm-defense system of Cimex lectularius and its implications for pest management(2015) Ulrich, Kevin Richard; Thorne, Barbara L; Entomology; Digital Repository at the University of Maryland; University of Maryland (College Park, Md.)In this dissertation, I focus on the alarm-defense system of the common bed bug, Cimex lectularius, its effectiveness against pathogen attacks, and its role as a mechanism of communication for conspecifics. This dual role of an alarm-defense system is efficient and effective considering that the two functions are typically required simultaneously in times of danger; the same substance should serve both purposes. First, I surveyed the most common types of commercial bed bug treatments to determine long-term efficacy. Regardless of the treatment, chemical or heat, retreatments for bed bug infestations were required. After 3 years, 20.8% of housing units receiving a chemical treatment required additional treatments; 9.5% of units receiving heat treatments required a retreatment during the same period. Multifamily units required retreatments significantly more than all other housing types. Given these findings that emphasize the necessity for a multifaceted IPM program, I investigated whether the entomopathogenic fungus, Metarhizium anisopliae, could be used to control bed bugs. Feeding experiments demonstrated that bed bugs were innately susceptible to this fungus. However, regardless of whether bed bugs were sprayed with a fungal solution or contacted a treated surface, only at 98% humidity was mortality high. In addition, the two major aldehydes (E)-2-hexenal and (E)-2-octenal emitted as defensive secretions by bed bugs inhibited the in vitro growth of an isolate of M. anisopliae. The ability to accurately and quickly detect new infestations is a critical element to an IPM-based strategy. This detection requires an understanding of attraction behavior and cues. I show through use of video-tracking software, (E)-2-hexenal and (E)-2-octenal attract adult bed bugs. Behavioral assays determined both males and females were attracted to 0.04 ug of an aldehyde blend for up to two hours after initial treatment of filter paper disks. Results suggest that these bed bug secretions may be candidates for lures and monitors. Taken together, this research describes the chemical ecology of bed bugs, providing insight into relevant signaling and defensive behavior, which has direct implications on pest management practices.