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The waggle dance of the honey bee (Apis mellifera L.) is perhaps the most celebrated animal communication behavior. With a waggle dance, a forager bee who has discovered a profitable resource on the landscape, usually floral nectar or pollen, can inform her nestmates of its location and recruit them to exploit it by communicating both a distance and a direction. Since Karl von Frisch described the waggle dance in 1942, scientific exploration of the dance has exploded into the realms of its structure, function, role in the regulation of collective foraging in the context of the hive as a super-organism, and even its utility as a study system for understanding sublethal behavioral effects of pesticide exposure. This dissertation presents three novel studies of the waggle dance. In the first, we asked whether consistent inter-bee differences (i.e., individuality) in a waggle dance distance - duration calibrations could affect communication success. In the second, we characterized the networks of recruitment arising from waggle dance communications and explored the role of the aforementioned individuality in network formation. In the third, we tested whether sublethal exposure to glyphosate (GLY), the most-applied herbicide in the world, could affect foraging, recruitment, or the levels and balance of biogenic amines in the bee brain. In each of these experiments, we housed bees in clear-walled observation colonies and trained cohorts of bees to visit artificial feeders to record both foraging and recruitment data. In our first experiment, we found that individuality in waggle dance behavior does shape communication outcomes, indicating that individual-level behavioral differences should not be discounted as factors at work in eusocial insect societies. In the second, we present the first network density and dance burstiness data from in vivo bee networks, revealing that recruitment networks are sparse, and waggle dancers are partitioned into bursty and non-bursty behavioral types. In the third, we show that not only can sublethal GLY exposure reduce foraging, but it can also produce significant correlations between levels of the important insect neurotransmitter octopamine and its two biosynthetic precursors, tyramine and tyrosine, where levels in control bees were unrelated. The results of this dissertation research, while distinct by experiment, together emphasize the continuing usefulness and tractability of the honey bee colony as a system in which to study the role of individuality in animal communication and to better understand the threat posed by non-insecticidal pesticide chemistries to the planet's most economically impactful pollinator. / Doctor of Philosophy / One of the most famous and well-studied animal behaviors is the waggle dance of the honey bee. A honey bee's waggle dance works similarly to a Yelp review for a restaurant: a bee who has found a good food source, like a flower patch offering especially sweet nectar or high-quality pollen, can come back to the colony and recommend it to her nestmates with a dance. The waggle dance is even more specific than a Yelp review, however, in that it also gives instructions to find the food source, communicating both a distance and a direction so that dance followers can go out into the landscape and look for the food source themselves. Even though the waggle dance has been studied extensively since it was first described by Karl von Frisch in the 1940s, there are still unknowns about how it works, and how it might be impacted by certain stressors. This dissertation presents three different experiments aimed at shedding light on these unknowns. First, it has recently been shown that there are consistent differences between bees in the way they communicate distance in the dance, and we tested whether that between-bee individuality can affect the likelihood that two bees will communicate successfully. Second, we studied how information about a food source moves from bee to bee via the waggle dance to form a communication network. Specifically, we described how efficiently information moved from bee to bee, patterns of dancing behavior, and the role of that individuality in its formation. Third and lastly, we looked to see whether exposure to a weedkiller called glyphosate (GLY) could affect either honey bees' waggle dance or food-collecting behavior, as well as levels of certain neurotransmitters in their brains that are involved in those behaviors. In all three experiments, we collected our data by housing bees in a clear-walled observation hives that let us view and film their waggle dance behavior, and then training groups of bees to collect artificial nectar from a feeder station that we provided, so we could also observe them as they collected food. We found that individuality in waggle dance communication can indeed affect the likelihood of communication success between two given bees, where the likelihood of communication success is greater when the dancer communicates a farther distance to the food source than the follower would. In the second experiment, our study of the waggle dance communication network showed that (1) information does not flow from bee to bee very efficiently, and (2) bees either dance quite regularly or sporadically. As far as we know, we are the first to describe these aspects of the waggle dance communication network, which may be useful in the field of computing algorithms inspired by living organisms. Finally, our third experiment showed that mild GLY exposure not only reduced how frequently bees collected food from our feeder, but also changed the relative amounts of certain neurotransmitters in their brains. This result emphasizes the importance of understanding how weedkillers that are not meant to target beneficial insects like honey bees are actually affecting them, so that we can make better-informed decisions to protect honey bees and other good insects.

abstract: Vitellogenin (Vg) is an ancient and highly conserved multifunctional protein. It is primarily known for its role in egg-yolk formation but also serves functions pertaining to immunity, longevity, nutrient storage, and oxidative stress relief. In the honey bee (Apis mellifera), Vg has evolved still further to include important social functions that are critical to the maintenance and proliferation of colonies. Here, Vg is used to synthesize royal jelly, a glandular secretion produced by a subset of the worker caste that is fed to the queen and young larvae and which is essential for caste development and social immunity. Moreover, Vg in the worker caste sets the pace of their behavioral development as they transition between different tasks throughout their life. In this dissertation, I make several new discoveries about Vg functionality. First, I uncover a colony-level immune pathway in bees that uses royal jelly as a vehicle to transfer pathogen fragments between nestmates. Second, I show that Vg is localized and expressed in the honey bee digestive tract and suggest possible immunological functions it may be performing there. Finally, I show that Vg enters to nucleus and binds to deoxyribonucleic acid (DNA), acting as a potential transcription factor to regulate expression of many genes pertaining to behavior, metabolism, and signal transduction pathways. These findings represent a significant advance in the understanding of Vg functionality and honey bee biology, and set the stage for many future avenues of research. / Dissertation/Thesis / Doctoral Dissertation Evolutionary Biology 2019

<p>    </p> <p>Domestication is the process by which a previously wild population is managed by humans, thereby being subjected to a different set of selective pressures than experienced in its natural setting. Its opposite, feralization, is therefore when a domesticate escapes or is released from a captive setting, reasserting natural selective pressures. The genomics underpinning both domesti- cation and feralization have not been studied in insects; the Western honey bee (<em>Apis mellifera </em>L.) is a good model for this system, as honey bees exist in both a managed and feral state, and have extensive historic and genomic resources to document population changes. My goal in this thesis was to 1) improve upon our understanding of honey bee importation and genetics to the United States to support demographic assertions, and 2) to sequence managed and feral stocks of honey bees to identify the population structure and 3) genetic differences underpinning domestication. Ultimately, I reconstructed 400 years of honey bee importation and management history, creating the most comprehensive understanding to date of importation dates and locations, historical man- agement practices, and genetic bottlenecks. Additionally, I summarized thirty years of honey bee genome sequencing to provide a road map for future studies. Then, I conducted whole genome pooled sequencing on six managed and three feral stocks of honey bees from the United States. The mitochondrial and whole genome ancestry of feral colonies holds relics from their importation history, while managed colonies show evidence of more recent importation events. The managed stocks in my sample set have higher overall genetic diversity, but exhibit little differentiation, but feral stocks exhibit varying levels of differentiation, indicating different levels of ferality likely dictated by the level of reproductive isolation from managed colonies. </p>

Honey bees utilize their circadian rhythms to accurately predict the time of day. This ability allows foragers to remember the specific timing of food availability and its location for several days. Previous studies have provided strong evidence toward light/dark cycles being the primary Zeitgeber for honey bees. Work in our laboratory described large individual variation in the endogenous period length of honey bee foragers from the same colony and differences in the endogenous rhythms under different constant temperatures. In this study, we further this work by examining the temperature inside the honey bee colony. By placing temperature and light data loggers at different locations inside the colony we measured temperature at various locations within the colony. We observed significant oscillations of the temperature inside the hive, that show seasonal patterns. We then simulated the observed temperature oscillations in the laboratory and found that using the temperature cycle as a Zeitgeber, foragers present large individual differences in the phase of locomotor rhythms for temperature. Moreover, foragers successfully synchronize their locomotor rhythms to these simulated temperature cycles. Advancing the cycle by six hours, resulting in changes in the phase of activity in some foragers in the assay. The results are shown in this study highlight the importance of temperature as a potential Zeitgeber in the field. Future studies will examine the possible functional and evolutionary role of the observed phase differences of circadian rhythms.

The honey bee is one of the most important crop pollinating insects in the world. Researchers have recently identified a disease that has begun to impact the honey bee population. Colony Collapse Disorder results in the death of many bee colonies every year, but the cause for this remains unknown. Investigating the cause, harmonic radars are being considered to track the foraging patterns of honey bees. This research endeavors to find an optimized waveform for use in tracking foraging bees. Harmonic oscillators were developed for a transmit frequency of 1.2 GHz and various waveforms were tested against the oscillators. Ultimately, the waveform was found to be arbitrary. The amount of power that the harmonic oscillator receives is the determining factor. Given this, a general pulsed waveform can be developed that attempts to provide the maximum possible return for a predetermined maximum range of interest.

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Honeybees (Apis mellifera L.) are the major insect pollinators of many different crops. A drastic decline in the honey bee populations has been reported over the past decade. While many factors have contributed to this decline, pesticides, poor nutrition, and Varroa mites are the most common concerns noted by scientists and beekeepers. Aside from direct toxicity from pesticides, it has been observed that sublethal pesticide doses have effects on honey bee physiology and behavior such as oxidative stress, disruption of foraging and homing, and changes to honey bee neurophysiology. The primary objectives of this project were to examine honey bee gut microbiome, physiology, and pesticide exposure along an agricultural intensification gradient and to examine the interactive impacts of pesticide exposure and poor nutrition on honey bees in a controlled laboratory cage setting. Sixteen honey bee colonies were placed in four locations across Mississippi with varying degrees of natural forage availability.

Body size is a universal property affecting biological structure and function, from cell metabolism to animal behavior. The nervous system, the physical generator of behavior, is also affected by variations in body size; hence potentially affecting the way animals perceive, interpret and react to the environment. When animals join to form groups, such individual differences become part of the structure of the society, even determining social roles. Here, I explore the association between body size, behavior and social organization in honeybees and bumblebees. Focusing on bumblebees, I explore the link between body size, brain allometry and learning and memory performance, within the context of task specialization. I show that body size goes along with brain size and with learning and memory performance, and that foraging experience affects such cognitive and neural features. Next, I explore the association between body size and foraging task specialization in honeybees. Previous evidence showed a link between specialization on pollen or nectar foraging and sensory sensitivity, further associating sensitivity to the quality and/or quantity of resource exploited. I hypothesize that, as in solitary bees, larger body size is associated with higher sensory sensitivity. I test this hypothesis by comparing body size and the quality and quantity of the resource exploited by wild Africanized and European honeybees. I show that nectar foragers are smaller and have fewer olfactory sensilla, which might underlie their lower sensitivity to odors. Also, larger bees collect more pollen (within pollen foragers) and more dilute nectar (within nectar foragers). To further test this `size hypothesis', I compare strains of bees selected to store large ("high strain") or small ("low strain") amounts of pollen surplus. As these strains differ in sensory sensitivity, I predict that the more sensitive high strain bees are larger and have more sensory sensilla. I show that high strain bees are generally bigger, but have fewer sensory sensilla than low strain bees. These results show that in bees, body size is associated with an individual's sensory, neural and cognitive features, further suggesting that body size plays a more important role in the organization of bee societies than generally assumed.

Animals in general vary immensely in body size, which greatly affects their morphology, physiology, survival, and nutritional requirements. The nervous system is also affected by variation in body size, which, in turn, shapes the perception of environmental stimuli and the behavior of animals. Comparative studies of vertebrates suggest that larger brains and their integrative centers comprise more and generally larger neurons (Jerison, 1973; Kaas, 2000), but much less is known about brain - body size relations in invertebrates. Closely related social bee species are well suited to study correlations between body size and brain composition. Different honey bee species vary in body size yet differ little in their ecological requirements and behavior and bumble bees feature a large range of body sizes even within a single colony.