The Foundress’s Dilemma: Group Selection for Cooperation Among Queens of the Harvester Ant, Pogonomyrmex Californicus

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Description

The evolution of cooperation is a fundamental problem in biology, especially for non-relatives, where indirect fitness benefits cannot counter within-group inequalities. Multilevel selection models show how cooperation can evolve if it generates a group-level advantage, even when cooperators are disadvantaged

The evolution of cooperation is a fundamental problem in biology, especially for non-relatives, where indirect fitness benefits cannot counter within-group inequalities. Multilevel selection models show how cooperation can evolve if it generates a group-level advantage, even when cooperators are disadvantaged within their group. This allows the possibility of group selection, but few examples have been described in nature. Here we show that group selection can explain the evolution of cooperative nest founding in the harvester ant Pogonomyrmex californicus. Through most of this species’ range, colonies are founded by single queens, but in some populations nests are instead founded by cooperative groups of unrelated queens. In mixed groups of cooperative and single-founding queens, we found that aggressive individuals had a survival advantage within their nest, but foundress groups with such non-cooperators died out more often than those with only cooperative members. An agent-based model shows that the between-group advantage of the cooperative phenotype drives it to fixation, despite its within-group disadvantage, but only when population density is high enough to make between-group competition intense. Field data show higher nest density in a population where cooperative founding is common, consistent with greater density driving the evolution of cooperative foundation through group selection.

Date Created
2016-07-28
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The Aims and Structures of Research Projects That Use Gene Regulatory Information with Evolutionary Genetic Models

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Description
At the interface of developmental biology and evolutionary biology, the very

criteria of scientific knowledge are up for grabs. A central issue is the status of evolutionary genetics models, which some argue cannot coherently be used with complex gene regulatory network

At the interface of developmental biology and evolutionary biology, the very

criteria of scientific knowledge are up for grabs. A central issue is the status of evolutionary genetics models, which some argue cannot coherently be used with complex gene regulatory network (GRN) models to explain the same evolutionary phenomena. Despite those claims, many researchers use evolutionary genetics models jointly with GRN models to study evolutionary phenomena.

How do those researchers deploy those two kinds of models so that they are consistent and compatible with each other? To address that question, this dissertation closely examines, dissects, and compares two recent research projects in which researchers jointly use the two kinds of models. To identify, select, reconstruct, describe, and compare those cases, I use methods from the empirical social sciences, such as digital corpus analysis, content analysis, and structured case analysis.

From those analyses, I infer three primary conclusions about projects of the kind studied. First, they employ an implicit concept of gene that enables the joint use of both kinds of models. Second, they pursue more epistemic aims besides mechanistic explanation of phenomena. Third, they don’t work to create and export broad synthesized theories. Rather, they focus on phenomena too complex to be understood by a common general theory, they distinguish parts of the phenomena, and they apply models from different theories to the different parts. For such projects, seemingly incompatible models are synthesized largely through mediated representations of complex phenomena.

The dissertation closes by proposing how developmental evolution, a field traditionally focused on macroevolution, might fruitfully expand its research agenda to include projects that study microevolution.
Date Created
2017
Agent

Heliconius in a new light: the effects of light environments on mimetic coloration, behavior, and visual systems

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Although mimetic animal coloration has been studied since Darwin's time, many questions on the efficacy, evolution, and function of mimicry remain unanswered. Müller (1879) hypothesized that unpalatable individuals converge on the same conspicuous coloration to reduce predation. However, there are

Although mimetic animal coloration has been studied since Darwin's time, many questions on the efficacy, evolution, and function of mimicry remain unanswered. Müller (1879) hypothesized that unpalatable individuals converge on the same conspicuous coloration to reduce predation. However, there are many cases where closely related, unpalatable species have diverged from a shared conspicuous pattern. What selection pressures have led to divergence in warning colors? Environmental factors such as ambient light have been hypothesized to affect signal transmission and efficacy in animals. Using two mimetic pairs of Heliconius butterflies, Postman and Blue-white, I tested the hypothesis that animals with divergent mimetic colors segregate by light environment to maximize conspicuousness of the aposematic warning signal under their particular environmental conditions. Each mimetic pair was found in a light environment that differed in brightness and spectral composition, which affected visual conspicuousness differently depending on mimetic color patch. I then used plasticine models in the field to test the hypothesis that mimics had higher survival in the habitat where they occurred. Although predation rates differed between the two habitats, there was no interactive effect of species by habitat type. Through choice experiments, I demonstrated that mimetic individuals preferred to spend time in the light environment where they were most often found and that their absolute visual sensitivity corresponds to the ambient lighting of their respective environment. Eye morphology was then studied to determine if differences in total corneal surface area and/or facet diameters explained the differences in visual sensitivities, but the differences found in Heliconius eye morphology did not match predictions based upon visual sensitivity. To further understand how eye morphology varies with light environments, I studied many tropical butterflies from open and closed habitats to reveal that forest understory butterflies have larger facets compared to butterflies occupying open habitats. Lastly, I tested avian perception of mimicry in a putative Heliconius mimetic assemblage and show that the perceived mimetic resemblance depends upon visual system. This dissertation reveals the importance of light environments on mimicry, coloration, behavior and visual systems of tropical butterflies.
Date Created
2016
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A context-dependent alarm signal in the ant Temnothorax rugatulus

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Description
Because collective cognition emerges from local signaling among group members, deciphering communication systems is crucial to understanding the underlying mechanisms. Alarm signals are widespread in the social insects and can elicit a variety of behavioral responses to danger, but the

Because collective cognition emerges from local signaling among group members, deciphering communication systems is crucial to understanding the underlying mechanisms. Alarm signals are widespread in the social insects and can elicit a variety of behavioral responses to danger, but the functional plasticity of these signals has not been well studied. Here we report an alarm pheromone in the ant Temnothorax rugatulus that elicits two different behaviors depending on context. When an ant was tethered inside an unfamiliar nest site and unable to move freely, she released a pheromone from her mandibular gland that signaled other ants to reject this nest as a potential new home, presumably to avoid potential danger. When the same pheromone was presented near the ants' home nest, they were instead attracted to it, presumably to respond to a threat to the colony. We used coupled gas chromatography/mass spectrometry to identify candidate compounds from the mandibular gland and tested each one in a nest choice bioassay. We found that 2,5-dimethylpyrazine was sufficient to induce rejection of a marked new nest and also to attract ants when released at the home nest. This is the first detailed investigation of chemical communication in the leptothoracine ants. We discuss the possibility that this pheromone's deterrent function can improve an emigrating colony's nest site selection performance.
Date Created
2014-09-01
Agent

Design of Ant-Inspired Stochastic Control Policies for Collective Transport by Robotic Swarms

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In this paper, we present an approach to designing decentralized robot control policies that mimic certain microscopic and macroscopic behaviors of ants performing collective transport tasks. In prior work, we used a stochastic hybrid system model to characterize the observed

In this paper, we present an approach to designing decentralized robot control policies that mimic certain microscopic and macroscopic behaviors of ants performing collective transport tasks. In prior work, we used a stochastic hybrid system model to characterize the observed team dynamics of ant group retrieval of a rigid load. We have also used macroscopic population dynamic models to design enzyme-inspired stochastic control policies that allocate a robotic swarm around multiple boundaries in a way that is robust to environmental variations. Here, we build on this prior work to synthesize stochastic robot attachment–detachment policies for tasks in which a robotic swarm must achieve non-uniform spatial distributions around multiple loads and transport them at a constant velocity. Three methods are presented for designing robot control policies that replicate the steady-state distributions, transient dynamics, and fluxes between states that we have observed in ant populations during group retrieval. The equilibrium population matching method can be used to achieve a desired transport team composition as quickly as possible; the transient matching method can control the transient population dynamics of the team while driving it to the desired composition; and the rate matching method regulates the rates at which robots join and leave a load during transport. We validate our model predictions in an agent-based simulation, verify that each controller design method produces successful transport of a load at a regulated velocity, and compare the advantages and disadvantages of each method.

Date Created
2014-12-01
Agent

Decoding brood pheromone: the releaser and primer effects of young and old larvae on honey bee (Apis mellifera) workers

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How a colony regulates the division of labor to forage for nutritional resources while accommodating for changes in colony demography is a fundamental question in the sociobiology of social insects. In honey bee, Apis mellifera, brood composition impacts the division

How a colony regulates the division of labor to forage for nutritional resources while accommodating for changes in colony demography is a fundamental question in the sociobiology of social insects. In honey bee, Apis mellifera, brood composition impacts the division of labor, but it is unknown if colonies adjust the allocation of foragers to carbohydrate and protein resources based on changes in the age demography of larvae and the pheromones they produce. Young and old larvae produce pheromones that differ in composition and volatility. In turn, nurses differentially provision larvae, feeding developing young worker larvae a surplus diet that is more queen-like in protein composition and food availability, while old larvae receive a diet that mimics the sugar composition of the queen larval diet but is restrictively fed instead of provided ad lib. This research investigated how larval age and the larval pheromone e-β ocimene (eβ) impact foraging activity and foraging load. Additional cage studies were conducted to determine if eβ interacts synergistically with queen mandibular pheromone (QMP) to suppress ovary activation and prime worker physiology for nursing behavior. Lastly, the priming effects of larval age and eβ on worker physiology and the transition from in-hive nursing tasks to outside foraging were examined. Results indicate that workers differentially respond to larvae of different ages, likely by detecting changes in the composition of the pheromones they emit. This resulted in adjustments to the foraging division of labor (pollen vs. nectar) to ensure that the nutritional needs of the colony's brood were met. For younger larvae and eβ, this resulted in a bias favoring pollen collection. The cage studies reveal that both eβ and QMP suppressed ovary activation, but the larval pheromone was more effective. Maturing in an environment of young or old larvae primed bees for nursing and impacted important endocrine titers involved in the transition to foraging, so bees maturing in the presence of larvae foraged earlier than control bees reared with no brood.
Date Created
2014
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Visual Navigation During Colony Emigration by the Ant 'Temnothorax Rugatulus'

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Description

Many ants rely on both visual cues and self-generated chemical signals for navigation, but their relative importance varies across species and context. We evaluated the roles of both modalities during colony emigration by Temnothorax rugatulus. Colonies were induced to move

Many ants rely on both visual cues and self-generated chemical signals for navigation, but their relative importance varies across species and context. We evaluated the roles of both modalities during colony emigration by Temnothorax rugatulus. Colonies were induced to move from an old nest in the center of an arena to a new nest at the arena edge. In the midst of the emigration the arena floor was rotated 60 degrees around the old nest entrance, thus displacing any substrate-bound odor cues while leaving visual cues unchanged. This manipulation had no effect on orientation, suggesting little influence of substrate cues on navigation. When this rotation was accompanied by the blocking of most visual cues, the ants became highly disoriented, suggesting that they did not fall back on substrate cues even when deprived of visual information. Finally, when the substrate was left in place but the visual surround was rotated, the ants' subsequent headings were strongly rotated in the same direction, showing a clear role for visual navigation. Combined with earlier studies, these results suggest that chemical signals deposited by Temnothorax ants serve more for marking of familiar territory than for orientation. The ants instead navigate visually, showing the importance of this modality even for species with small eyes and coarse visual acuity.

Date Created
2013-08-30
Agent

The genetics of speciation in the parasitoid wasp, Nasonia

Description
Speciation is the fundamental process that has generated the vast diversity of life on earth. The hallmark of speciation is the evolution of barriers to gene flow. These barriers may reduce gene flow either by keeping incipient species from hybridizing

Speciation is the fundamental process that has generated the vast diversity of life on earth. The hallmark of speciation is the evolution of barriers to gene flow. These barriers may reduce gene flow either by keeping incipient species from hybridizing at all (pre-zygotic), or by reducing the fitness of hybrids (post-zygotic). To understand the genetic architecture of these barriers and how they evolve, I studied a genus of wasps that exhibits barriers to gene flow that act both pre- and post-zygotically. Nasonia is a genus of four species of parasitoid wasps that can be hybridized in the laboratory. When two of these species, N. vitripennis and N. giraulti are mated, their offspring suffer, depending on the generation and cross examined, up to 80% mortality during larval development due to incompatible genic interactions between their nuclear and mitochondrial genomes. These species also exhibit pre-zygotic isolation, meaning they are more likely to mate with their own species when given the choice. I examined these two species and their hybrids to determine the genetic and physiological bases of both speciation mechanisms and to understand the evolutionary forces leading to them. I present results that indicate that the oxidative phosphorylation (OXPHOS) pathway, an essential pathway that is responsible for mitochondrial energy generation, is impaired in hybrids of these two species. These results indicate that this impairment is due to the unique evolutionary dynamics of the combined nuclear and mitochondrial origin of this pathway. I also present results showing that, as larvae, these hybrids experience retarded growth linked to the previously observed mortality and I explore possible physiological mechanisms for this. Finally, I show that the pre-mating isolation is due to a change in a single pheromone component in N. vitripennis males, that this change is under simple genetic control, and that it evolved neutrally before being co-opted as a species recognition signal. These results are an important addition to our overall understanding of the mechanisms of speciation and showcase Nasonia as an emerging model for the study of the genetics of speciation.
Date Created
2013
Agent

Egg policing and fertility signaling across colony development in the ant Camponotus floridanus

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Description
Of all the signals and cues that orchestrate the activities of a social insect colony, the reproductives' fertility pheromones are perhaps the most fundamental. These pheromones regulate reproductive division of labor, a defining characteristic of eusociality. Despite their critical role,

Of all the signals and cues that orchestrate the activities of a social insect colony, the reproductives' fertility pheromones are perhaps the most fundamental. These pheromones regulate reproductive division of labor, a defining characteristic of eusociality. Despite their critical role, reproductive fertility pheromones are not evenly expressed across the development of a social insect colony and may even be absent in the earliest colony stages. In the ant Camponotus floridanus, queens of incipient colonies do not produce the cuticular hydrocarbons that serve as fertility and egg-marking signals in this species. My dissertation investigates the consequences of the dramatic change in the quantity of these pheromones that occurs as the colony grows. C. floridanus workers from large, established colonies use egg surface hydrocarbons to discriminate among eggs. Eggs with surface hydrocarbons typical of eggs laid by established queens are nurtured, whereas eggs lacking these signals (i.e., eggs laid by workers and incipient queens) are destroyed. I characterized how workers from incipient colonies responded to eggs lacking queen fertility hydrocarbons. I found that established-queen-laid eggs, incipient-queen-laid eggs, and worker-laid eggs were not destroyed by workers at this colony stage. Destruction of worker-laid eggs is a form of policing, and theoretical models predict that policing should be strongest in incipient colonies. Since there was no evidence of policing by egg-eating in incipient C. floridanus colonies, I searched for evidence of another policing mechanism at this colony stage. Finding none, I discuss reasons why policing behavior may not be expressed in incipient colonies. I then considered the mechanism that accounts for the change in workers' response to eggs. By manipulating ants' egg experience and testing their egg-policing decisions, I found that ants use a combination of learned and innate criteria to discriminate between targets of care and destruction. Finally, I investigated how the increasing strength of queen-fertility hydrocarbons affects nestmate recognition, which also relies on cuticular hydrocarbons. I found that queens with strong fertility hydrocarbons can be transferred between established colonies without aggression, but they cannot be introduced into incipient colonies. Queens from incipient colonies cannot be transferred into incipient or established colonies.
Date Created
2012
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A practical and theoretical approach to understanding the selective mechanisms behind genetic caste determination in Pogonomyrmex rugosus and Pogonomyrmex barbatus

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Description
Gene-centric theories of evolution by natural selection have been popularized and remain generally accepted in both scientific and public paradigms. While gene-centrism is certainly parsimonious, its explanations fall short of describing two patterns of evolutionary and social phenomena: the evolution

Gene-centric theories of evolution by natural selection have been popularized and remain generally accepted in both scientific and public paradigms. While gene-centrism is certainly parsimonious, its explanations fall short of describing two patterns of evolutionary and social phenomena: the evolution of sex and the evolution of social altruism. I review and analyze current theories on the evolution of sex. I then introduce the conflict presented to gene-centric evolution by social phenomena such as altruism and caste sterility in eusocial insects. I review gene-centric models of inclusive fitness and kin selection proposed by Hamilton and Maynard Smith. Based their assumptions, that relatedness should be equal between sterile workers and reproductives, I present several empirical examples that conflict with their models. Following that, I introduce a unique system of genetic caste determination (GCD) observed in hybrid populations of two sister-species of seed harvester ants, Pogonomyrmex rugosus and Pogonomyrmex barbatus. I review the evidence for GCD in those species, followed by a critique of the current gene-centric models used to explain it. In chapter two I present my own theoretical model that is both simple and extricable in nature to explain the origin, evolution, and maintenance of GCD in Pogonomyrmex. Furthermore, I use that model to fill in the gaps left behind by the contributing authors of the other GCD models. As both populations in my study system formed from inter-specific hybridization, I review modern discussions of heterosis (also called hybrid vigor) and use those to help explain the ecological competitiveness of GCD. I empirically address the inbreeding depression the lineages of GCD must overcome in order to remain ecologically stable, demonstrating that as a result of their unique system of caste determination, GCD lineages have elevated recombination frequencies. I summarize and conclude with an argument for why GCD evolved under selective mechanisms which cannot be considered gene-centric, providing evidence that natural selection can effectively operate on non-heritable genotypes appearing in groups and other social contexts.
Date Created
2012
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