History dependence in insect flight decisions during odor tracking

Natural decision-making often involves extended decision sequences in response to variable stimuli with complex structure. As an example, many animals follow odor plumes to locate food sources or mates, but turbulence breaks up the advected odor signal into intermittent filaments and puffs. This scenario provides an opportunity to ask how animals use sparse, instantaneous, and stochastic signal encounters to generate goal-oriented behavioral sequences. Here we examined the trajectories of flying fruit flies (Drosophila melanogaster) and mosquitoes (Aedes aegypti) navigating in controlled plumes of attractive odorants. While it is known that mean odor-triggered flight responses are dominated by upwind turns, individual responses are highly variable. We asked whether deviations from mean responses depended on specific features of odor encounters, and found that odor-triggered turns were slightly but significantly modulated by two features of odor encounters. First, encounters with higher concentrations triggered stronger upwind turns. Second, encounters occurring later in a sequence triggered weaker upwind turns. To contextualize the latter history dependence theoretically, we examined trajectories simulated from three normative tracking strategies. We found that neither a purely reactive strategy nor a strategy in which the tracker learned the plume centerline over time captured the observed history dependence. In contrast, “infotaxis”, in which flight decisions maximized expected information gain about source location, exhibited a history dependence aligned in sign with the data, though much larger in magnitude. These findings suggest that while true plume tracking is dominated by a reactive odor response it might also involve a history-dependent modulation of responses consistent with the accumulation of information about a source over multi-encounter timescales. This suggests that short-term memory processes modulating decision sequences may play a role in natural plume tracking

History dependence in insect flight decisions during odor tracking

Natural decision-making often involves extended decision sequences in response to variable stimuli with complex structure. As an example, many animals follow odor plumes to locate food sources or mates, but turbulence breaks up the advected odor signal into intermittent filaments and puffs. This scenario provides an opportunity to ask how animals use sparse, instantaneous, and stochastic signal encounters to generate goal-oriented behavioral sequences. Here we examined the trajectories of flying fruit flies (Drosophila melanogaster) and mosquitoes (Aedes aegypti) navigating in controlled plumes of attractive odorants. While it is known that mean odor-triggered flight responses are dominated by upwind turns, individual responses are highly variable. We asked whether deviations from mean responses depended on specific features of odor encounters, and found that odor-triggered turns were slightly but significantly modulated by two features of odor encounters. First, encounters with higher concentrations triggered stronger upwind turns. Second, encounters occurring later in a sequence triggered weaker upwind turns. To contextualize the latter history dependence theoretically, we examined trajectories simulated from three normative tracking strategies. We found that neither a purely reactive strategy nor a strategy in which the tracker learned the plume centerline over time captured the observed history dependence. In contrast, “infotaxis”, in which flight decisions maximized expected information gain about source location, exhibited a history dependence aligned in sign with the data, though much larger in magnitude. These findings suggest that while true plume tracking is dominated by a reactive odor response it might also involve a history-dependent modulation of responses consistent with the accumulation of information about a source over multi-encounter timescales. This suggests that short-term memory processes modulating decision sequences may play a role in natural plume tracking

Algorithms for Olfactory Search across Species

Localizing the sources of stimuli is essential. Most organisms cannot eat, mate, or escape without knowing where the relevant stimuli originate. For many, if not most, animals, olfaction plays an essential role in search. While microorganismal chemotaxis is relatively well understood, in larger animals the algorithms and mechanisms of olfactory search remain mysterious. In this symposium, we will present recent advances in our understanding of olfactory search in flies and rodents. Despite their different sizes and behaviors, both species must solve similar problems, including meeting the challenges of turbulent airflow, sampling the environment to optimize olfactory information, and incorporating odor information into broader navigational systems

Life history tracking of social communication and navigation behaviors in honeybees (Apis mellifera L.)

The honeybee (Apis mellifera L.) is an ideal model for studying social behaviors and navigation. Social activities and navigational flights are two key aspects to regulate the function of social community. These complex processes usually involve dance communication, antennation, trophallaxis (social behaviors), and orientation and foraging flights (navigation). As group-living animals, honeybees are known to rely mainly on social information to help make decisions on whether, how and where to forage for food. However, honeybees may also constantly integrate their own experience with the information from other bees to make a final decision. Therefore, the degree to which bees follow the information from other individuals or apply their own knowledge would be age-dependent and experience-dependent on an individual basis. Meanwhile, honeybees, in particular living in a colony with small size, may be vulnerable to the external natural environment. There is no knowledge yet about how the development of the indoor and outdoor behaviors is and how the previously mentioned social and non-social factors influence bees’ behaviors indoors and outdoors, in particular how social behaviors influence the outdoor activities and vice versa. Therefore, the aim of the current study is to find the answers to these questions. This study combined the advantages of Raspberry Pi with video cameras by aid of infra-red illumination on one side, and harmonic radar on the other side to record the social behaviors inside of the colony without disruption and monitor flight trajectories outdoors in real-time. The social behaviors and flights were recorded over the bees’ lifetime within 15 days. In summary, each individual bee possesses their own rhythms with different levels of variation in responding to both social and non-social factors at both group and individual levels. The age dependence and experience dependence of the indoor and outdoor behaviors were found, however, of which the degrees of such dependence were various for different behaviors among different individuals and within an individual over the lifetime. Within the small community, my results showed that there was a small group of ‘elite’ bees that outperformed in both social interaction and flights, which in some sense reflect the collective characteristics and exquisite labor division in the eusocial community. Dance communication is known to convey vector information about the food sources that bees discover during foraging flights. Importantly, my studies firstly discovered that dance communication transmit both motivational and instructive role in the orientation and foraging flights, of which, the influence of information of direction and distance on the orientation and foraging flights in some degree was different. My result firstly discovered that dance communication plays important roles in both motivation and vector roles in bees’ orientation and foraging flights. Noise of information transfer is universal in dance communication. However, its influence on the orientation and foraging flights were not similar which depended on the different purposes of orientation and foraging flights. Honeybees could selectively determine to use flight information form dance communication. For the future, I suggest collecting more datasets about social behaviors to enrich the current conclusions. However, this is critically necessary to rely on an automatically tracking method with high accuracy and fast computing speed.Die Honigbiene (Apis mellifera L.) ist ein idealer Modellorganismus zur Untersuchung des Sozialverhaltens und der Navigation. Soziale Aktivitäten und Navigationsflüge sind zwei Schlüsselaspekte, die das Funktionieren der sozialen Gemeinschaft regeln. Zu diesen komplexen Prozessen gehören die Tanzkommunikation, Antennation und Trophallaxis (Sozialverhalten) sowie Orientierungs- und Sammelflüge (Navigation). Als in Gruppen lebende Tiere verlassen sich Honigbienen bekanntermaßen hauptsächlich auf soziale Informationen, um zu entscheiden, ob, wie und wo sie auf Nahrungssuche gehen. Allerdings können Honigbienen auch unentwegt ihre eigenen Erfahrungen mit den Informationen anderer Bienen kombinieren, um eine endgültige Entscheidung zu treffen. Inwieweit Bienen den Informationen anderer Individuen folgen oder ihr eigenes Wissen anwenden, ist daher individuell alters- und erfahrungsabhängig. In der Zwischenzeit sind Honigbienen, insbesondere wenn sie in einem kleinen Volk leben, anfällig für die äußere natürliche Umgebung sein. Es gibt noch keine Erkenntnisse darüber, wie sich das Verhalten in innerhalb und außerhalb des Volkes entwickelt und wie die zuvor genannten sozialen und nicht-sozialen Faktoren das Verhalten der Bienen innerhalb und außerhalb beeinflussen, insbesondere wie das soziale Verhalten die Aktivitäten im Freien beeinflusst und umgekehrt. Ziel der vorliegenden Studie ist es daher, Antworten auf diese Fragen zu finden. In dieser Studie wurden die Vorteile des Raspberry Pi mit Videokameras mit Hilfe von Infrarot-Beleuchtung auf der einen Seite und harmonischem Radar auf der anderen Seite kombiniert, um das Sozialverhalten innerhalb der Kolonie ohne Unterbrechung aufzuzeichnen und die Flugbahnen im Freien in Echtzeit zu überwachen. Das Sozialverhalten und die Flüge wurden über die gesamte Lebensdauer der Bienen innerhalb von 15 Tagen aufgezeichnet. Zusammenfassend hat jede einzelne Biene ihren eigenen Rhythmus, der sowohl auf Gruppen- als auch auf Individualebene unterschiedlich stark auf soziale und nicht- soziale Faktoren reagiert. Es wurde eine Alters- und Erfahrungsabhängigkeit des Innen- und Außenverhaltens festgestellt, wobei das Ausmaß dieser Abhängigkeit für verschiedene Verhaltensweisen bei verschiedenen Individuen und innerhalb eines Individuums im Laufe des Lebens unterschiedlich war. Innerhalb der kleinen Gemeinschaft des Versuchsstockes zeigten meine Ergebnisse, dass es eine kleine Gruppe von "Elite"-Bienen gab, die sowohl bei der sozialen Interaktion als auch bei den Flügen die Leistungen anderer übertrafen, was in gewisser Weise die kollektiven Merkmale und die exquisite Arbeitsteilung in der eusozialen Gemeinschaft widerspiegelt. Weiter ist bekannt, dass die Tanzkommunikation Vektorinformationen über die Nahrungsquellen vermittelt, die die Bienen während ihrer Flüge zur Futtersuche entdecken. Bedeutsam ist, dass meine Studien zunächst zeigen, dass die Tanzkommunikation sowohl eine motivierende als auch eine anweisende Rolle bei der Orientierung und den Futterflügen spielt, wobei der Einfluss von Richtungs- und Entfernungsinformationen auf die Orientierungs- und Sammelflüge zu einem gewissen Maße unterschiedlich war. Meine Ergebnisse zeigen weiterhin, dass die Tanzkommunikation sowohl eine motivierende als auch eine weisende Rolle bei den Orientierungs- und Sammelflügen der Bienen spielt. Ein Rauschen ist universell in der Informationsübertragung der Tanzkommunikation. Der Einfluss auf die Orientierungs- und Suchflüge war jedoch nicht gleich, was von den unterschiedlichen Zielen der Orientierungs- und Sammelflüge abhing. Honigbienen konnten selektiv entscheiden, ob sie Fluginformationen aus der Tanzkommunikation verwenden. Für zukünftige Studien schlage ich vor, weitere Datensätze über das Sozialverhalten zusammen um die aktuellen Schlussfolgerungen zu ergänzen. Dazu ist es jedoch unbedingt erforderlich, sich auf eine automatische Trackingmethode mit hoher Genauigkeit und schneller Rechengeschwindigkeit zu stützen

Odor stimuli: not just chemical identity

No description supplie

Odour-mediated host seeking and discrimination in mosquitoes : chemistry, neurobiology and behaviour

The majority of the world’s population is at risk of one or more mosquito-borne diseases that are transmitted by blood-feeding female mosquitoes, affecting both human health and economic development. Especially Anopheles gambiae, the principal malaria vector, and Aedes aegypti, the vector of dengue and yellow fever, are of primary concern due to their strong specialisation on human hosts, and the high number of casualties caused by the pathogens they transmit. Host seeking and discrimination are crucial for disease transmission, and are predominantly mediated by olfaction. Using a wind tunnel system and a custom analysis pipeline, this thesis confirms that the two mosquito species use volatile host cues, derived from breath and body, differentially, as carbon dioxide on its own drives host seeking in Ae. aegypti, but not in An. gambiae (paper I). To discriminate between host and nonhost species (paper V), Ae. aegypti encode human identity by the relative activation of two glomeruli within the antennal lobe, the primary olfactory centre, of which one is tuned to long-chain aldehydes enriched in human odour. A synthetic blend mimicking the glomerular activation elicited host seeking in Ae. aegypti (paper II). Next to preferring human over non-human hosts, Ae. aegypti also prefer some human individuals to others, which was demonstrated to be affected by the ABO blood type and pregnancy or menstrual cycle phase. Analysis of the volatiles associated with individual volunteers, identified 1-octen-3-ol to be significantly associated with very high attractiveness (paper III). The molecular regulation of host seeking acquisition during An. gambiae female adult maturation was independent of odorant receptor gene AgamOR39 expression (paper IV). The results presented in this thesis contribute to the understanding of mosquito host seeking and discrimination from multiple perspectives, which is a prerequisite to ultimately develop novel tools for mosquito monitoring and control

Larval Rearing Temperature Influences Amount and Composition of the Marking Pheromone of the Male Beewolf, Philanthus triangulum

Pheromones play an important role for courtship and mating in many insect species, and they are shaped by a complex interaction of genetic and environmental factors. Developmental temperature is known to have a strong influence on adult life history, morphology, and physiology, but little is known about its effect on pheromone characteristics. In the present study, the influence of temperature during larval development on the amount and composition of the complex marking pheromone from the cephalic glands of the adult male beewolf, Philanthus triangulum F. (Hymenoptera: Crabronidae), was investigated. Additionally, the effects of temperature on several life-history traits were examined. European beewolf larvae were reared at three constant temperatures (20, 25, and 30° C). Males reared at 20° C showed longer development times and higher mortality, suggesting that low temperatures constitute stressful conditions for developing larvae. After eclosion, the amount and composition of the scent marking secretion of the adult males was analyzed by coupled gas chromatography-mass spectrometry. Males that had been reared at 20° C had significantly less secretion than individuals reared under warmer conditions (25° C and 30° C). Furthermore, larval rearing temperature had a significant effect on the composition of the adult males' pheromone gland content, with warmer rearing conditions leading to higher relative amounts of compounds with high molecular weight. The results show that the temperature during larval development significantly affected the amount and composition of the content of the male pheromone glands, probably due to physiological constraints and competing processes for limited energetic resources. Thus, the pheromone gland content may contain information on developmental conditions of males, which may have consequences for female mate choice decisions and male reproductive success

Representations of Reward and Movement in Drosophila Dopaminergic Neurons

The neuromodulator dopamine is known to influence both immediate and future behavior, motivating and invigorating an animal’s ongoing movement but also serving as a reinforcement signal to instruct learning. Yet it remains unclear whether this dual role of dopamine involves the same dopaminergic pathways. Although reward-responsive dopaminergic neurons display movement-related activity, debate continues as to what features of an individual’s experience these motor-correlates correspond and how they influence concurrent behavior. The mushroom body, a prominent neuropil in the brain of the fruit fly Drosophila melanogaster, is richly innervated by dopaminergic neurons that play an essential role in the formation of olfactory associations. While dopaminergic neurons respond to reward and punishment to drive associative learning, they have also been implicated in a number of adaptive behaviors and their activity correlates with the behavioral state of an animal and its coarse motor actions. Here, we take advantage of the concise circuit architecture of the Drosophila mushroom body to investigate the nature of motor-related signals in dopaminergic neurons that drive associative learning. In vivo functional imaging during naturalistic tethered locomotion reveals that the activity of different subsets of mushroom body dopaminergic neurons reflects distinct aspects of movement. To gain insight into what facets of an animal’s experience are represented by these movement-related signals, we employed a closed loop virtual reality paradigm to monitor neural activity as animals track an olfactory stimulus and are actively engaged in a goal-directed and sensory-motivated behavior. We discover that odor responses in dopaminergic neurons correlate with the extent to which an animal tracks upwind towards the fictive odor source. In different experimental contexts where distinct motor actions were required to track the odor, dopaminergic neurons become emergently linked to the behavioral metric most relevant for effective olfactory navigation. Subsets of dopaminergic neurons were correlated with the strength of upwind tracking regardless of the identity of the odor and remained so even after the satiety state of an animal was altered. We proceed to demonstrate that transient inhibition of dopaminergic neurons that are positively correlated with upwind tracking significantly diminishes the normal approach responses to an appetitive olfactory cue. Accordingly, activation of those same dopaminergic neurons enhances approach to an odor and even drives upwind tracking in clean air alone. Together, these results reveal that the same dopaminergic pathways that convey reinforcements to instruct learning also carry representations of an animal’s moment-by-moment movements and actively influence behavior. The complex activity patterns of mushroom body dopaminergic neurons therefore represent neither purely sensory nor motor variables but rather reflect the goal or motivation underlying an animal’s movements. Our data suggest a fundamental coupling between reinforcement signals and motivation-related locomotor representations within dopaminergic circuitry, drawing a striking parallel between the mushroom body dopaminergic neurons described here and the emerging understanding of mammalian dopaminergic pathways. The apparent conservation in dopaminergic neuromodulatory networks between mammals and insects suggests a shared logic for how neural circuits assign meaning to both sensory stimuli and motor actions to generate flexible and adaptive behavior

Behavioral and molecular mechanisms of pheromone transmission in the honey bee (Apis mellifera)

The European honey bee (Apis mellifera) has a sophisticated system of pheromonal signals that mediate a wide range of behaviors important for their fitness, including reproductive dominance, nest defense, and cooperative brood care. In honey bees, there are two distinct pheromones emitted by larvae, brood pheromone and (E)-beta-ocimene. By integrating behavior, chemical ecology, and transcriptomics, this dissertation analyzes several key stages in signal transmission in a systematic effort to understand how these two pheromones affect behavior, and in the process, generates a synthetic understanding of a highly complex system of communication. Previous studies have explored behavioral and gene expression patterns related to honey bee pheromones; however, none have compared the roles that two divergent pheromones from a common source play in rapid regulation of foraging behavior. Furthermore, while previous studies have investigated the mechanisms of pheromone detection and the factors involved in regulation of foraging behavior, it remains unclear how individual responses to pheromone exposure scales to colony-level changes in behavior. By investigating the behavioral, physiological, and genomic influences of honey bee chemical communication, this dissertation links phenotypic plasticity in behavior to gene expression profiles in the brain and provides insights into the evolution of a sophisticated chemical language.Ecology, Evolution and Behavio