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- All Subjects: Biology
- Creators: Fewell, Jennifer H
Description
There is increasing evidence that ovarian status influcences behavioral phenotype in workers of the honey bee Apis mellifera. Honey bee workers demonstrate a complex division of labor. Young workers perform in-hive tasks (e.g. brood care), while older bees perform outside tasks (e.g. foraging for food). This age correlated division of labor is known as temporal polyethism. Foragers demonstrate further division of labor with some bees biasing collection towards protein (pollen) and others towards carbohydrates (nectar). The Reproductive Ground-plan Hypothesis proposes that the ovary plays a regulatory role in foraging division of labor. European honey bee workers that have been selectively bred to store larger amounts of pollen (High strain) also have a higher number of ovarioles per ovary than workers from strains bred to store less pollen (Low strain). High strain bees also initiate foraging earlier than Low strain bees. The relationship between ovariole number and foraging behavior is also observed in wild-type Apis mellifera and Apis cerana: pollen-biased foragers have more ovarioles than nectar-biased foragers. In my first study, I investigated the pre-foraging behavioral patterns of the High and Low strain bees. I found that High strain bees progress through the temporal polyethism at a faster rate than Low strain bees. To ensure that the observed relationship between the ovary and foraging bias is not due to associated separate genes for ovary size and foraging behavior, I investigated foraging behavior of African-European backcross bees. The backcross breeding program was designed to break potential gene associations. The results from this study demonstrated the relationship between the ovary and foraging behavior, supporting the proposed causal linkage between reproductive development and behavioral phenotype. The final study was designed to elucidate a regulatory mechanism that links ovariole number with sucrose sensitivity, and loading decisions. I measured ovariole number, sucrose sensitivity and sucrose solution load size using a rate-controlled sucrose delivery system. I found an interaction effect between ovariole number and sucrose sensitivity for sucrose solution load size. This suggests that the ovary impacts carbohydrate collection through modulation of sucrose sensitivity. Because nectar and pollen collection are not independent, this would also impact protein collection.
ContributorsSiegel, Adam J (Author) / Page, Jr., Robert E (Thesis advisor) / Hamilton, Andrew L. (Committee member) / Brent, Colin S (Committee member) / Amdam, Gro V (Committee member) / McGraw, Kevin J. (Committee member) / Arizona State University (Publisher)
Created2011
Description
Social insect colonies exhibit striking diversity in social organization. Included in this overwhelming variation in structure are differences in colony queen number. The number of queens per colony varies both intra- and interspecifically and has major impacts on the social dynamics of a colony and the fitness of its members. To understand the evolutionary transition from single to multi-queen colonies, I examined a species which exhibits variation both in mode of colony founding and in the queen number of mature colonies. The California harvester ant Pogonomyrmex californicus exhibits both variation in the number of queens that begin a colony (metrosis) and in the number of queens in adult colonies (gyny). Throughout most of its range, colonies begin with one queen (haplometrosis) but in some populations multiple queens cooperate to initiate colonies (pleometrosis). I present results that confirm co-foundresses are unrelated. I also map the geographic occurrence of pleometrotic populations and show that the phenomenon appears to be localized in southern California and Northern Baja California. Additionally, I provide genetic evidence that pleometrosis leads to primary polygyny (polygyny developing from pleometrosis) a phenomenon which has received little attention and is poorly understood. Phylogenetic and haplotype analyses utilizing mitochondrial markers reveal that populations of both behavioral types in California are closely related and have low mitochondrial diversity. Nuclear markers however, indicate strong barriers to gene flow between focal populations. I also show that intrinsic differences in queen behavior lead to the two types of populations observed. Even though populations exhibit strong tendencies on average toward haplo- or pleometrosis, within population variation exists among queens for behaviors relevant to metrosis and gyny. These results are important in understanding the dynamics and evolutionary history of a distinct form of cooperation among unrelated social insects. They also help to understand the dynamics of intraspecific variation and the conflicting forces of local adaptation and gene flow.
ContributorsOverson, Rick P (Author) / Gadau, Jürgen (Thesis advisor) / Fewell, Jennifer H (Committee member) / Hölldobler, Bert (Committee member) / Johnson, Robert A. (Committee member) / Liebig, Jürgen (Committee member) / Arizona State University (Publisher)
Created2011
Description
Division of labor, whereby different group members perform different functions, is a fundamental attribute of sociality. It appears across social systems, from simple cooperative groups to complex eusocial colonies. A core challenge in sociobiology is to explain how patterns of collective organization are generated. Theoretical models propose that division of labor self-organizes, or emerges, from interactions among group members and the environment; division of labor is also predicted to scale positively with group size. I empirically investigated the emergence and scaling of division of labor in evolutionarily incipient groups of sweat bees and in eusocial colonies of harvester ants. To test whether division of labor is an emergent property of group living during early social evolution, I created de novo communal groups of the normally solitary sweat bee Lasioglossum (Ctenonomia) NDA-1. A division of labor repeatedly arose between nest excavation and guarding tasks; results were consistent with hypothesized effects of spatial organization and intrinsic behavioral variability. Moreover, an experimental increase in group size spontaneously promoted higher task specialization and division of labor. Next, I examined the influence of colony size on division of labor in larger, more integrated colonies of the harvester ant Pogonomyrmex californicus. Division of labor scaled positively with colony size in two contexts: during early colony ontogeny, as colonies grew from tens to hundreds of workers, and among same-aged colonies that varied naturally in size. However, manipulation of colony size did not elicit a short-term response, suggesting that the scaling of division of labor in P. californicus colonies is a product of functional integration and underlying developmental processes, rather than a purely emergent epiphenomenon. This research provides novel insights into the organization of work in insect societies, and raises broader questions about the role of size in sociobiology.
ContributorsHolbrook, Carter Tate (Author) / Fewell, Jennifer H (Thesis advisor) / Gadau, Jürgen (Committee member) / Harrison, Jon F. (Committee member) / Hölldobler, Berthold (Committee member) / Johnson, Robert A. (Committee member) / Arizona State University (Publisher)
Created2011
Description
A notable feature of advanced eusocial insect groups is a division of labor within the sterile worker caste. However, the physiological aspects underlying the differentiation of behavioral phenotypes are poorly understood in one of the most successful social taxa, the ants. By starting to understand the foundations on which social behaviors are built, it also becomes possible to better evaluate hypothetical explanations regarding the mechanisms behind the evolution of insect eusociality, such as the argument that the reproductive regulatory infrastructure of solitary ancestors was co-opted and modified to produce distinct castes. This dissertation provides new information regarding the internal factors that could underlie the division of labor observed in both founding queens and workers of Pogonomyrmex californicus ants, and shows that changes in task performance are correlated with differences in reproductive physiology in both castes. In queens and workers, foraging behavior is linked to elevated levels of the reproductively-associated juvenile hormone (JH), and, in workers, this behavioral change is accompanied by depressed levels of ecdysteroid hormones. In both castes, the transition to foraging is also associated with reduced ovarian activity. Further investigation shows that queens remain behaviorally plastic, even after worker emergence, but the association between JH and behavioral bias remains the same, suggesting that this hormone is an important component of behavioral development in these ants. In addition to these reproductive factors, treatment with an inhibitor of the nutrient-sensing pathway Target of Rapamycin (TOR) also causes queens to become biased towards foraging, suggesting an additional sensory component that could play an important role in division of labor. Overall, this work provides novel identification of the possible regulators behind ant division of labor, and suggests how reproductive physiology could play an important role in the evolution and regulation of non-reproductive social behaviors.
ContributorsDolezal, Adam G (Author) / Amdam, Gro V (Thesis advisor) / Brent, Colin S. (Committee member) / Gadau, Juergen (Committee member) / Hoelldobler, Bert (Committee member) / Liebig, Juergen (Committee member) / Arizona State University (Publisher)
Created2012
Description
For interspecific mutualisms, the behavior of one partner can influence the fitness of the other, especially in the case of symbiotic mutualisms where partners live in close physical association for much of their lives. Behavioral effects on fitness may be particularly important if either species in these long-term relationships displays personality. Animal personality is defined as repeatable individual differences in behavior, and how correlations among these consistent traits are structured is termed behavioral syndromes. Animal personality has been broadly documented across the animal kingdom but is poorly understood in the context of mutualisms. My dissertation focuses on the structure, causes, and consequences of collective personality in Azteca constructor colonies that live in Cecropia trees, one of the most successful and prominent mutualisms of the neotropics. These pioneer plants provide hollow internodes for nesting and nutrient-rich food bodies; in return, the ants provide protection from herbivores and encroaching vines. I first explored the structure of the behavioral syndrome by testing the consistency and correlation of colony-level behavioral traits under natural conditions in the field. Traits were both consistent within colonies and correlated among colonies revealing a behavioral syndrome along a docile-aggressive axis. Host plants of more active, aggressive colonies had less leaf damage, suggesting a link between a colony personality and host plant health. I then studied how aspects of colony sociometry are intertwined with their host plants by assessing the relationship among plant growth, colony growth, colony structure, ant morphology, and colony personality. Colony personality was independent of host plant measures like tree size, age, volume. Finally, I tested how colony personality influenced by soil nutrients by assessing personality in the field and transferring colonies to plants the greenhouse under different soil nutrient treatments. Personality was correlated with soil nutrients in the field but was not influenced by soil nutrient treatment in the greenhouse. This suggests that soil nutrients interact with other factors in the environment to structure personality. This dissertation demonstrates that colony personality is an ecologically relevant phenomenon and an important consideration for mutualism dynamics.
ContributorsMarting, Peter (Author) / Pratt, Stephen C (Thesis advisor) / Wcislo, William T (Committee member) / Hoelldobler, Bert (Committee member) / Fewell, Jennifer H (Committee member) / Gadau, Juergen (Committee member) / Arizona State University (Publisher)
Created2018
Description
An important component of insect social structure is the number of queens that cohabitate in a colony. Queen number is highly variable between and within species. It can begin at colony initiation when often unrelated queens form cooperative social groups, a strategy known as primary polygyny. The non-kin cooperative groups formed by primary polygyny have profound effects on the social dynamics and inclusive fitness benefits within a colony. Despite this, the evolution of non-kin queen cooperation has been relatively overlooked in considerations of the evolution of cooperative sociality. To date, studies examining the costs and benefits of primary polygyny have focused primarily on the advantages of multiple queens during colony founding and early growth, but the impact of their presence extends to colony maturity and reproduction.
In this dissertation, I evaluate the ecological drivers and fitness consequences of non-kin queen cooperation, by comparing the reproduction of mature single-queen versus polygynous harvester ant (Pogonomyrmex californicus) colonies in the field. I captured and quantified the total number and biomass of reproductives across multiple mating seasons, comparing between populations that vary in the proportion of single queen versus polygynous colonies, to assess the fitness outcomes of queen cooperation. Colonies in a mainly polygynous site had lower reproductive investment than those in sites with predominantly single-queen colonies. The site dominated by polygyny had higher colony density and displayed evidence of resource limitation, pressures that may drive the evolution of queen cooperation.
I also used microsatellite markers to examine how polygynous queens share worker and reproductive production with nest-mate queens. The majority of queens fairly contribute to worker production and equally share reproductive output. However, there is a low frequency of queens that under-produce workers and over-produce reproductive offspring. This suggests that cheating by reproducing queens is possible, but uncommon. Competitive pressure from neighboring colonies could reduce the success of colonies that contain cheaters and maintain a low frequency of this phenotype in the population.
In this dissertation, I evaluate the ecological drivers and fitness consequences of non-kin queen cooperation, by comparing the reproduction of mature single-queen versus polygynous harvester ant (Pogonomyrmex californicus) colonies in the field. I captured and quantified the total number and biomass of reproductives across multiple mating seasons, comparing between populations that vary in the proportion of single queen versus polygynous colonies, to assess the fitness outcomes of queen cooperation. Colonies in a mainly polygynous site had lower reproductive investment than those in sites with predominantly single-queen colonies. The site dominated by polygyny had higher colony density and displayed evidence of resource limitation, pressures that may drive the evolution of queen cooperation.
I also used microsatellite markers to examine how polygynous queens share worker and reproductive production with nest-mate queens. The majority of queens fairly contribute to worker production and equally share reproductive output. However, there is a low frequency of queens that under-produce workers and over-produce reproductive offspring. This suggests that cheating by reproducing queens is possible, but uncommon. Competitive pressure from neighboring colonies could reduce the success of colonies that contain cheaters and maintain a low frequency of this phenotype in the population.
ContributorsHaney, Brian R (Author) / Fewell, Jennifer H (Thesis advisor) / Cole, Blaine J. (Committee member) / Gadau, Juergen (Committee member) / Hoelldobler, Bert (Committee member) / Rutowski, Ron L (Committee member) / Arizona State University (Publisher)
Created2017
Description
Bee communities form the keystone of many ecosystems through their pollination services. They are dynamic and often subject to significant changes due to several different factors such as climate, urban development, and other anthropogenic disturbances. As a result, the world has been experiencing a decline in bee diversity and abundance, which can have detrimental effects in the ecosystems they inhabit. One of the largest factors that impacts bees in today's world is the rapid urbanization of our planet, and it impacts the bee community in mixed ways. Not very much is understood about the bee communities that exist in urban habitats, but as urbanization is inevitably going to continue, knowledge on bee communities will need to strengthen. This study aims to determine the levels of variance in bee communities, considering multiple variables that bee communities can differ in. The following three questions are posed: do bee communities that are spatially separated differ significantly? Do bee communities that are separated by seasons differ significantly? Do bee communities that are separated temporally (by year, interannually) differ significantly? The procedure to conduct this experiment consists of netting and trapping bees at two sites at various times using the same methods. The data is then statistically analyzed for differences in abundance, richness, diversity, and species composition. After performing the various statistical analyses, it has been discovered that bee communities that are spatially separated, seasonally separated, or interannually separated do not differ significantly when it comes to abundance and richness. Spatially separated bee communities and interannually separated bee communities show a moderate level of dissimilarity in their species composition, while seasonally separated bee communities show a greater level of dissimilarity in species composition. Finally, seasonally separated bee communities demonstrate the greatest disparity of bee diversity, while interannually separated bee communities show the least disparity of bee diversity. This study was conducted over the time span of two years, and while the levels of variance of an urban area between these variables were determined, further variance studies of greater length or larger areas should be conducted to increase the currently limited knowledge of bee communities in urban areas. Additional studies on precipitation amounts and their effects on bee communities should be conducted, and studies from other regions should be taken into consideration while attempting to understand what is likely the most environmentally significant group of insects.
ContributorsPhan, James Thien (Author) / Sweat, Ken (Thesis director) / Foltz-Sweat, Jennifer (Committee member) / School of Music (Contributor) / School of Molecular Sciences (Contributor) / Barrett, The Honors College (Contributor)
Created2017-05
Description
A key factor in the success of social animals is their organization of work. Mathematical models have been instrumental in unraveling how simple, individual-based rules can generate collective patterns via self-organization. However, existing models offer limited insights into how these patterns are shaped by behavioral differences within groups, in part because they focus on analyzing specific rules rather than general mechanisms that can explain behavior at the individual-level. My work argues for a more principled approach that focuses on the question of how individuals make decisions in costly environments.
In Chapters 2 and 3, I demonstrate how this approach provides novel insights into factors that shape the flexibility and robustness of task organization in harvester ant colonies (Pogonomyrmex barbatus). My results show that the degree to which colonies can respond to work in fluctuating environments depends on how individuals weigh the costs of activity and update their behavior in response to social information. In Chapter 4, I introduce a mathematical framework to study the emergence of collective organization in heterogenous groups. My approach, which is based on the theory of multi-agent systems, focuses on myopic agents whose behavior emerges out of an independent valuation of alternative choices in a given work environment. The product of this dynamic is an equilibrium organization in which agents perform different tasks (or abstain from work) with an analytically defined set of threshold probabilities. The framework is minimally developed, but can be extended to include other factors known to affect task decisions including individual experience and social facilitation. This research contributes a novel approach to developing (and analyzing) models of task organization that can be applied in a broader range of contexts where animals cooperate.
In Chapters 2 and 3, I demonstrate how this approach provides novel insights into factors that shape the flexibility and robustness of task organization in harvester ant colonies (Pogonomyrmex barbatus). My results show that the degree to which colonies can respond to work in fluctuating environments depends on how individuals weigh the costs of activity and update their behavior in response to social information. In Chapter 4, I introduce a mathematical framework to study the emergence of collective organization in heterogenous groups. My approach, which is based on the theory of multi-agent systems, focuses on myopic agents whose behavior emerges out of an independent valuation of alternative choices in a given work environment. The product of this dynamic is an equilibrium organization in which agents perform different tasks (or abstain from work) with an analytically defined set of threshold probabilities. The framework is minimally developed, but can be extended to include other factors known to affect task decisions including individual experience and social facilitation. This research contributes a novel approach to developing (and analyzing) models of task organization that can be applied in a broader range of contexts where animals cooperate.
ContributorsUdiani, Oyita (Author) / Kang, Yun (Thesis advisor) / Fewell, Jennifer H (Thesis advisor) / Janssen, Marcus A (Committee member) / Castillo-Chavez, Carlos (Committee member) / Arizona State University (Publisher)
Created2016
Description
Understanding how and why animals choose what to eat is one of the fundamental goals of nutritional and behavioral biology. This question can be scaled to animals that live in social groups, including eusocial insects. One of the factors that plays an important role in foraging decisions is the prevalence of specific nutrients and their relative balance. This dissertation explores the role of relative nutrient content in the food selection decisions of a species that is eusocial and also agricultural, the desert leafcutter ant Acromyrmex versicolor. A dietary choice assay, in which the relative amount of protein and carbohydrates in the available diets was varied, demonstrated that A. versicolor colonies regulate relative collection of protein and carbohydrates. Tracking the foraging behavior of individual workers revelaed that foragers vary in their relative collection of experimental diets and in their foraging frequency, but that there is no relationship between these key factors of foraging behavior. The high proportion of carbohydrates preferred by lab colonies suggests that they forage to nutritionally support the fungus rather than brood and workers. To test this, the relative amounts of 1) fungus, and 2) brood (larvae) was manipulated and foraging response was measured. Changing the amount of brood had no effect on foraging. Although decreasing the size of fungus gardens did not change relative P:C collection, it produced significant increases in caloric intake, supporting the assertion that the fungus is the main driver of colony nutrient regulation. The nutritional content of naturally harvested forage material collected from field colonies was measured, as was recruitment to experimental diets with varying relative macronutrient content. Field results confirmed a strong colony preference for high carbohydrate diets. They also indicated that this species may, at times, be limited in its ability to collect sufficiently high levels of carbohydrates to meet optimal intake. This dissertation provides important insights about fundamental aspects of leafcutter ant biology and extends our understanding of the role of relative nutrient content in foraging decisions to systems that span multiple trophic levels.
ContributorsSmith, Nathan Edward (Author) / Fewell, Jennifer H (Thesis advisor) / Harrison, Jon F (Committee member) / Pavlic, Ted (Committee member) / Cease, Arianne (Committee member) / Hoelldobler, Bert (Committee member) / Arizona State University (Publisher)
Created2023
Description
Social insect groups, such as bees, termites, and ants, epitomize the emergence of group-level behaviors from the aggregated actions and interactions of individuals. Ants have the unique advantage that whole colonies can be observed in artificial, laboratory nests, and each individual's behavior can be continuously tracked using imaging software. In this dissertation, I study two group behaviors: (1) the spread of alarm signals from three agitated ants to a group of 61 quiescent nestmates, and (2) the reduction in per-capita energy use as colonies scale in size from tens of ants to thousands. For my first experiment, I track the motion of Pogonomyrmex californicus ants using an overhead camera, and I analyze how propagation of an initial alarm stimulus affects their walking speeds. I then build an agent-based model that simulates two-dimensional ant motion and the spread of the alarmed state. I find that implementing a simple set of rules for motion and alarm signal transmission reproduces the empirically observed speed dynamics. For the second experiment, I simulate social insect colony workers that collectively complete a set of tasks. By assuming that task switching is energetically costly, my model recovers a metabolic rate scaling pattern, known as hypometric metabolic scaling. This relationship, which predicts an organism's metabolic rate from its mass, is observed across a diverse set of social insect groups and animal species. The results suggest an explicit link between the degree of workers' task specialization and whole-colony energy use.
ContributorsLin, Michael Robert (Author) / Milner, Fabio A (Thesis advisor, Committee member) / Fewell, Jennifer H (Thesis advisor, Committee member) / Lampert, Adam (Committee member) / Arizona State University (Publisher)
Created2021