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1.  Layered Social Network Analysis Reveals Complex Relationships in Kindergarteners 
The interplay between individuals forms building blocks for social structure. Here, we examine the structure of behavioral interactions among kindergarten classroom with a hierarchy-neutral approach to examine all possible underlying patterns in the formation of layered networks of “reciprocal” interactions. To understand how these layers are coordinated, we used a layered motif approach. Our dual layered motif analysis can therefore be thought of as the dynamics of smaller groups that tile to create the group structure, or alternatively they provide information on what the average child would do in a given local social environment. When we examine the regulated motifs in layered networks, we find that transitivity is at least partially involved in the formation of these layered network structures. We also found complex combinations of the expected reciprocal interactions. The mechanisms used to understand social networks of kindergarten children here are also applicable on a more general scale to any group of individuals where interactions and identities can be readily observed and scored.
PMCID: PMC4773607  PMID: 26973572
hierarchy; social; kindergarten children; social structure; layered networks; motifs
2.  The nutritional and hedonic value of food modulate sexual receptivity in Drosophila melanogaster females 
Scientific Reports  2016;6:19441.
Food and sex often go hand in hand because of the nutritional cost of reproduction. For Drosophila melanogaster females, this relationship is especially intimate because their offspring develop on food. Since yeast and sugars are important nutritional pillars for Drosophila, availability of these foods should inform female reproductive behaviours. Yet mechanisms coupling food and sex are poorly understood. Here we show that yeast increases female sexual receptivity through interaction between its protein content and its odorous fermentation product acetic acid, sensed by the Ionotropic odorant receptor neuron Ir75a. A similar interaction between nutritional and hedonic value applies to sugars where taste and caloric value only increase sexual receptivity when combined. Integration of nutritional and sensory values would ensure that there are sufficient internal nutrients for egg production as well as sufficient environmental nutrients for offspring survival. These findings provide mechanisms through which females may maximize reproductive output in changing environments.
PMCID: PMC4726014  PMID: 26777264
3.  Socially synchronized circadian oscillators 
Daily rhythms of physiology and behaviour are governed by an endogenous timekeeping mechanism (a circadian ‘clock’). The alternation of environmental light and darkness synchronizes (entrains) these rhythms to the natural day–night cycle, and underlying mechanisms have been investigated using singly housed animals in the laboratory. But, most species ordinarily would not live out their lives in such seclusion; in their natural habitats, they interact with other individuals, and some live in colonies with highly developed social structures requiring temporal synchronization. Social cues may thus be critical to the adaptive function of the circadian system, but elucidating their role and the responsible mechanisms has proven elusive. Here, we highlight three model systems that are now being applied to understanding the biology of socially synchronized circadian oscillators: the fruitfly, with its powerful array of molecular genetic tools; the honeybee, with its complex natural society and clear division of labour; and, at a different level of biological organization, the rodent suprachiasmatic nucleus, site of the brain's circadian clock, with its network of mutually coupled single-cell oscillators. Analyses at the ‘group’ level of circadian organization will likely generate a more complex, but ultimately more comprehensive, view of clocks and rhythms and their contribution to fitness in nature.
PMCID: PMC3712435  PMID: 23825203
Drosophila; honeybee; suprachiasmatic nucleus; coupling; social synchronization; entrainment
4.  Pigment-Dispersing Factor Modulates Pheromone Production in Clock Cells that Influence Mating in Drosophila 
Neuron  2013;79(1):54-68.
Social cues contribute to the circadian entrainment of physiological and behavioral rhythms. These cues supplement the influence of daily and seasonal cycles in light and temperature. In Drosophila, the social environment modulates circadian mechanisms that regulate sex pheromone production and mating behavior. Here we demonstrate that a neuroendocrine pathway, defined by the neuropeptide Pigment-Dispersing Factor (PDF), couples the central nervous system (CNS) to the physiological output of peripheral clock cells that produce pheromones, the oenocytes. PDF signaling from the CNS modulates the phase of the oenocyte clock. Despite its requirement for sustaining free-running locomoter activity rhythms, PDF is not necessary to sustain molecular rhythms in the oenocytes. Interestingly, disruption of the PDF signaling pathway reduces male sex pheromones and results in sex-specific differences in mating behavior. Our findings highlight the role of neuropeptide signaling and the circadian system in synchronizing the physiological and behavioral processes which govern social interactions.
PMCID: PMC3955580  PMID: 23849197
5.  Drosophila melanogaster females change mating behaviour and offspring production based on social context 
In Drosophila melanogaster, biological rhythms, aggression and mating are modulated by group size and composition. However, the fitness significance of this group effect is unknown. By varying the composition of groups of males and females, we show that social context affects reproductive behaviour and offspring genetic diversity. Firstly, females mating with males from the same strain in the presence of males from a different strain are infecund, analogous to the Bruce effect in rodents, suggesting a social context-dependent inbreeding avoidance mechanism. Secondly, females mate more frequently in groups composed of males from more than one strain; this mitigates last male sperm precedence and increases offspring genetic diversity. However, smell-impaired Orco mutant females do not increase mating frequency according to group composition; this indicates that social context-dependent changes in reproductive behaviour depend on female olfaction, rather than direct male–male interactions. Further, variation in mating frequency in wild-type strains depends on females and not males. The data show that group composition can affect variance in the reproductive success of its members, and that females play a central role in this process. Social environment can thus influence the evolutionary process.
PMCID: PMC3350680  PMID: 22298851
Drosophila melanogaster; social behaviour; reproduction; mate choice; sperm competition; Bruce effect
6.  Hierarchical chemosensory regulation of male-male social interactions in Drosophila 
Nature neuroscience  2011;14(6):757-762.
Pheromones regulate male social behaviors in Drosophila, but the identities and behavioral role(s) of these chemosensory signals, and how they interact, are incompletely understood. Here we show that (Z)-7-tricosene (7-T), a male-enriched cuticular hydrocarbon (CH) previously shown to inhibit male-male courtship, is also essential for normal levels of aggression. The opposite influences of 7-T on aggression and courtship are independent, but both require the gustatory receptor Gr32a. Surprisingly, sensitivity to 7-T is required for the aggression-promoting effect of 11-cis-vaccenyl acetate (cVA), an olfactory pheromone, but 7-T sensitivity is independent of cVA. 7-T and cVA therefore regulate aggression in a hierarchical manner. Furthermore, the increased courtship caused by depletion of male CHs is suppressed by a mutation in the olfactory receptor Or47b. Thus, male social behaviors are controlled by gustatory pheromones that promote and suppress aggression and courtship, respectively, and whose influences are dominant to olfactory pheromones that enhance these behaviors.
PMCID: PMC3102769  PMID: 21516101
7.  Correction: Pheromonal and Behavioral Cues Trigger Male-to-Female Aggression in Drosophila 
PLoS Biology  2010;8(12):10.1371/annotation/1c19d040-9f9f-4b9f-b678-70f1fe387192.
PMCID: PMC2997046
8.  Pheromonal and Behavioral Cues Trigger Male-to-Female Aggression in Drosophila 
PLoS Biology  2010;8(11):e1000541.
By genetically manipulating both pheromonal profiles and behavioral patterns, we find that Drosophila males showed a complete reversal in their patterns of aggression towards other males and females
Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.
Author Summary
As in other species, the fruit fly Drosophila melanogaster uses chemical signals in the form of pheromones to recognize the species and sex of another individual. Males typically fight with other males and do not attack females. While the roles of pheromonal and other sensory cues in stimulating courtship towards females have been extensively studied, the signals that elicit aggression towards other males remain unclear. In this work, we use genetic tools to show that masculinization of female pheromones is sufficient to trigger aggression from wild type males towards females. Surprisingly, males also attacked females that displayed male patterns of aggression, even if they show normal female pheromonal profiles, indicating that pheromones are not the only cues important for identifying another animal as an opponent. By simultaneously manipulating pheromones and behavioral patterns of opponents, we can completely switch the behavioral response of males towards females and males. These results demonstrate that not only pheromonal but also behavioral cues can serve as triggers of aggression, underlining the importance of behavioral feedback in the manifestation of social behaviors.
PMCID: PMC2990703  PMID: 21124886
9.  Sequential Learning of Pheromonal Cues Modulates Memory Consolidation in Trainer-Specific Associative Courtship Conditioning 
Current biology : CB  2005;15(3):194-206.
Associative memory formation requires that animals choose predictors for experiences they need to remember. When an artificial odor is paired with an aversive experience, that odor becomes the predictor. In more natural settings, however, animals can have multiple salient experiences that need to be remembered and prioritized. The mechanisms by which animals deal with multiple experiences are incompletely understood.
Here we show that Drosophila males can be trained to discriminate between different types of female pheromones; they suppress courtship specifically to the type of female that was associated with unsuccessful courtship. Such “trainer-specific” learning is mediated by hydrocarbon olfactory cues and modifies the male’s processing of those cues. Animals that are unable to use olfactory cues can still learn by using other sensory modalities, but memory in this case is not specific to the trainer female’s maturation state. Concurrent and serial presentation of different pheromones demonstrates that the ability to consolidate memory of pheromonal cues can be modified by the temporal order in which they appear.
Suppression of memory by new learning demonstrates that the dynamics of memory consolidation are subject to plasticity in Drosophila. This type of metaplasticity is essential for navigation of experience-rich natural environments.
PMCID: PMC2805828  PMID: 15694302
10.  Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate 
Current biology : CB  2007;17(7):599-605.
Reproductive behavior in Drosophila has both stereotyped and plastic components that are driven by age- and sex-specific chemical cues. Males who unsuccessfully court virgin females subsequently avoid females that are of the same age as the trainer. In contrast, males trained with mature mated females associate volatile appetitive and aversive pheromonal cues and learn to suppress courtship of all females. Here we show that the volatile aversive pheromone that leads to generalized learning with mated females is (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA). cVA is a major component of the male cuticular hydrocarbon profile, but it is not found on virgin females. During copulation, cVA is transferred to the female in ejaculate along with sperm and peptides that decrease her sexual receptivity. When males sense cVA (either synthetic or from mated female or male extracts) in the context of female pheromone, they develop a generalized suppression of courtship. The effects of cVA on initial courtship of virgin females can be blocked by expression of tetanus toxin in Or65a, but not Or67d neurons, demonstrating that the aversive effects of this pheromone are mediated by a specific class of olfactory neuron. These findings suggest that transfer of cVA to females during mating may be part of the male’s strategy to suppress reproduction by competing males.
PMCID: PMC1913718  PMID: 17363250
Learning and memory; olfaction; Drosophila; pheromones; cis-vaccenyl acetate
11.  Advanced analysis of a cryptochrome mutation's effects on the robustness and phase of molecular cycles in isolated peripheral tissues of Drosophila 
BMC Neuroscience  2002;3:5.
Previously, we reported effects of the cryb mutation on circadian rhythms in period and timeless gene expression within isolated peripheral Drosophila tissues. We relied on luciferase activity driven by the respective regulatory genomic elements to provide real-time reporting of cycling gene expression. Subsequently, we developed a tool kit for the analysis of behavioral and molecular cycles. Here, we use these tools to analyze our earlier results as well as additional data obtained using the same experimental designs.
Isolated antennal pairs, heads, bodies, wings and forelegs were evaluated under light-dark cycles. In these conditions, the cryb mutation significantly decreases the number of rhythmic specimens in each case except the wing. Moreover, among those specimens with detectable rhythmicity, mutant rhythms are significantly weaker than cry+ controls. In addition, cryb alters the phase of period gene expression in these tissues. Furthermore, peak phase of luciferase-reported period and timeless expression within cry+ samples is indistinguishable in some tissues, yet significantly different in others. We also analyze rhythms produced by antennal pairs in constant conditions.
These analyses further show that circadian clock mechanisms in Drosophila may vary in a tissue-specific manner, including how the cry gene regulates circadian gene expression.
PMCID: PMC103668  PMID: 11960556
12.  Signal analysis of behavioral and molecular cycles 
BMC Neuroscience  2002;3:1.
Circadian clocks are biological oscillators that regulate molecular, physiological, and behavioral rhythms in a wide variety of organisms. While behavioral rhythms are typically monitored over many cycles, a similar approach to molecular rhythms was not possible until recently; the advent of real-time analysis using transgenic reporters now permits the observations of molecular rhythms over many cycles as well. This development suggests that new details about the relationship between molecular and behavioral rhythms may be revealed. Even so, behavioral and molecular rhythmicity have been analyzed using different methods, making such comparisons difficult to achieve. To address this shortcoming, among others, we developed a set of integrated analytical tools to unify the analysis of biological rhythms across modalities.
We demonstrate an adaptation of digital signal analysis that allows similar treatment of both behavioral and molecular data from our studies of Drosophila. For both types of data, we apply digital filters to extract and clarify details of interest; we employ methods of autocorrelation and spectral analysis to assess rhythmicity and estimate the period; we evaluate phase shifts using crosscorrelation; and we use circular statistics to extract information about phase.
Using data generated by our investigation of rhythms in Drosophila we demonstrate how a unique aggregation of analytical tools may be used to analyze and compare behavioral and molecular rhythms. These methods are shown to be versatile and will also be adaptable to further experiments, owing in part to the non-proprietary nature of the code we have developed.
PMCID: PMC65508  PMID: 11825337
13.  Drosophila Free-Running Rhythms Require Intercellular Communication 
PLoS Biology  2003;1(1):e13.
Robust self-sustained oscillations are a ubiquitous characteristic of circadian rhythms. These include Drosophila locomotor activity rhythms, which persist for weeks in constant darkness (DD). Yet the molecular oscillations that underlie circadian rhythms damp rapidly in many Drosophila tissues. Although much progress has been made in understanding the biochemical and cellular basis of circadian rhythms, the mechanisms that underlie the differences between damped and self-sustaining oscillations remain largely unknown. A small cluster of neurons in adult Drosophila brain, the ventral lateral neurons (LNvs), is essential for self-sustained behavioral rhythms and has been proposed to be the primary pacemaker for locomotor activity rhythms. With an LNv-specific driver, we restricted functional clocks to these neurons and showed that they are not sufficient to drive circadian locomotor activity rhythms. Also contrary to expectation, we found that all brain clock neurons manifest robust circadian oscillations of timeless and cryptochrome RNA for many days in DD. This persistent molecular rhythm requires pigment-dispersing factor (PDF), an LNv-specific neuropeptide, because the molecular oscillations are gradually lost when Pdf01 mutant flies are exposed to free-running conditions. This observation precisely parallels the previously reported effect on behavioral rhythms of the Pdf01 mutant. PDF is likely to affect some clock neurons directly, since the peptide appears to bind to the surface of many clock neurons, including the LNvs themselves. We showed that the brain circadian clock in Drosophila is clearly distinguishable from the eyes and other rapidly damping peripheral tissues, as it sustains robust molecular oscillations in DD. At the same time, different clock neurons are likely to work cooperatively within the brain, because the LNvs alone are insufficient to support the circadian program. Based on the damping results with Pdf01 mutant flies, we propose that LNvs, and specifically the PDF neuropeptide that it synthesizes, are important in coordinating a circadian cellular network within the brain. The cooperative function of this network appears to be necessary for maintaining robust molecular oscillations in DD and is the basis of sustained circadian locomotor activity rhythms.
Circadian rhythms are characterized by robust molecular oscillations, which are shown here to require a brain region-specific neuropeptide, PDF, for maintenance and coordination
PMCID: PMC193604  PMID: 12975658

Results 1-13 (13)