Drosophila typically move toward light (phototax positively) when startled. The various species of Drosophila exhibit some variation in their respective mean phototactic behaviors; however, it is not clear to what extent genetically identical individuals within each species behave idiosyncratically. Such behavioral individuality has indeed been observed in laboratory arthropods; however, the neurobiological factors underlying individual-to-individual behavioral differences are unknown. We developed "FlyVac," a high-throughput device for automatically assessing phototaxis in single animals in parallel. We observed surprising variability within every species and strain tested, including identically reared, isogenic strains. In an extreme example, a domesticated strain of Drosophila simulans harbored both strongly photopositive and strongly photonegative individuals. The particular behavior of an individual fly is not heritable and, because it persists for its lifetime, constitutes a model system for elucidating the molecular mechanisms of personality. Although all strains assayed had greater than expected variation (assuming binomial sampling), some had more than others, implying a genetic basis. Using genetics and pharmacology, we identified the metabolite transporter White and white-dependent serotonin as suppressors of phototactic personality. Because we observed behavioral idiosyncrasy in all experimental groups, we suspect it is present in most behaviors of most animals.ethology | stochasticity | bet-hedging | Ischnopterapion virens F ew debates in biology have generated broader interest than nature versus nurture. Not surprisingly, both heritable and environmental factors play significant roles in shaping an organism's traits. However, the precise contributions of genetic and environmental factors to complex traits, such as most behaviors, are poorly understood. Behavioral individuality, in the absence of genetic variation, has indeed been observed in the laboratory. Specifically, clonal pea aphids were shown to vary in their predator escape behavior, and these differences were maintained for at least 5 d (1). In another example, the naïve odor preference of fruit flies was highly variable across individuals (2). These experiments suggest that even when deterministic influences from genetics and environment are held constant, there is nevertheless considerable behavioral variability. Drosophila is an ideal model system to test whether individuals, matched both genetically and environmentally, possess unique behavioral personalities, and what genetic and neurobiological factors control the magnitude of this idiosyncrasy.To determine whether individuals are behaving idiosyncratically we need to measure the trial-to-trial variation in an individual's behavior and compare that to the variation between individuals. If we observe greater variability between individuals than within individuals (that cannot be explained by sampling error), this would constitute evidence for behavioral idiosyncrasy. This analysis req...
Genetically identical individuals display variability in their physiology, morphology, and behaviors, even when reared in essentially identical environments, but there is little mechanistic understanding of the basis of such variation. Here, we investigated whether Drosophila melanogaster displays individual-toindividual variation in locomotor behaviors. We developed a new high-throughout platform capable of measuring the exploratory behavior of hundreds of individual flies simultaneously. With this approach, we find that, during exploratory walking, individual flies exhibit significant bias in their left vs. right locomotor choices, with some flies being strongly left biased or right biased. This idiosyncrasy was present in all genotypes examined, including wild-derived populations and inbred isogenic laboratory strains. The biases of individual flies persist for their lifetime and are nonheritable: i.e., mating two left-biased individuals does not yield left-biased progeny. This locomotor handedness is uncorrelated with other asymmetries, such as the handedness of gut twisting, leg-length asymmetry, and wing-folding preference. Using transgenics and mutants, we find that the magnitude of locomotor handedness is under the control of columnar neurons within the central complex, a brain region implicated in motor planning and execution. When these neurons are silenced, exploratory laterality increases, with more extreme leftiness and rightiness. This observation intriguingly implies that the brain may be able to dynamically regulate behavioral individuality.behavior | individuality | personality | circuit mapping | central complex H and dominance-better performance using either the left or right hand-is a familiar human trait, moderately heritable (1), and regulated by many genes (2), including those involved in general body symmetry (3). However, behavioral handedness in general, i.e., the preferential performance of a behavior on one side of the body or with a particular chiral twist, is a multifaceted phenomenon. For example, in the absence of visual feedback, people display clockwise or counterclockwise biases in their walking behavior (4). This "locomotor handedness" is uncorrelated to hand dominance or gross morphological asymmetry and instead may be due to asymmetries in the collection and processing of sensory information, resulting in individual locomotor biases with a neurological basis (4, 5).Handed behavioral tendencies specific to individuals are also prevalent throughout the animal kingdom and have been shown in species as disparate as mice (paw use) (6), octopi (eye use) (7), and tortoises (side rolled on during righting) (8). There is also evidence that, at the population mean level, some species of insects have handed behaviors and asymmetric neurophysiological patterns (9). However, there has been little investigation of the differences in handed behaviors among individuals of the same insect species, and the mechanisms by which asymmetries are instilled in behavior are unknown. Considering beha...
In Drosophila, most individual olfactory receptor neurons (ORNs) project bilaterally to both sides of the brain1,2. Having bilateral rather than unilateral projections may represent a useful redundancy. However, bilateral ORN projections to the brain should also compromise the ability to lateralize odors. Nevertheless, walking or flying Drosophila reportedly turn toward their more strongly stimulated antenna3-5. Here we show that each ORN spike releases ~40% more neurotransmitter from the axon branch ipsilateral to the soma, as compared to the contralateral branch. As a result, when an odor activates the antennae asymmetrically, ipsilateral central neurons begin to spike a few milliseconds before contralateral neurons, and ipsilateral central neurons also fire at a 30-50% higher rate. We show that a walking fly can detect a 5% asymmetry in total ORN input to its left and right antennal lobes, and can turn toward the odor in less time than it requires the fly to complete a stride. These results demonstrate that neurotransmitter release properties can be tuned independently at output synapses formed by a single axon onto two target cells with identical functions and morphologies. Our data also show that small differences in spike timing and spike rate can produce reliable differences in olfactory behavior.
Much remains unknown about how the nervous system of an animal generates behaviour, and even less is known about the evolution of behaviour. How does evolution alter existing behaviours or invent novel ones? Progress in computational techniques and equipment will allow these broad, complex questions to be explored in great detail. Here we present a method for tracking each leg of a fruit fly behaving spontaneously upon a trackball, in real time. Legs were tracked with infrared-fluorescent dyes invisible to the fly, and compatible with two-photon microscopy and controlled visual stimuli. We developed machine-learning classifiers to identify instances of numerous behavioural features (for example, walking, turning and grooming), thus producing the highest-resolution ethological profiles for individual flies.
To fully understand the mechanisms giving rise to behavior, we need to be able to precisely measure it. When coupled with large behavioral data sets, unsupervised clustering methods offer the potential of unbiased mapping of behavioral spaces. However, unsupervised techniques to map behavioral spaces are in their infancy, and there have been few systematic considerations of all the methodological options. We compared the performance of seven distinct mapping methods in clustering a wavelettransformed data set consisting of the x-and y-positions of the six legs of individual flies. Legs were automatically tracked by small pieces of fluorescent dye, while the fly was tethered and walking on an air-suspended ball. We find that there is considerable variation in the performance of these mapping methods, and that better performance is attained when clustering is done in higher dimensional spaces (which are otherwise less preferable because they are hard to visualize). High dimensionality means that some algorithms, including the non-parametric watershed cluster assignment algorithm, cannot be used. We developed an alternative watershed algorithm which can be used in high-dimensional spaces when a probability density estimate can be computed directly. With these tools in hand, we examined the behavioral space of fly leg postural dynamics and locomotion. We find a striking division of behavior into modes involving the fore legs and modes involving the hind legs, with few direct transitions between them. By computing behavioral clusters using the data from all flies simultaneously, we show that this division appears to be common to all flies. We also identify individual-to-individual differences in behavior and behavioral transitions. Lastly, we suggest a computational pipeline that can achieve satisfactory levels of performance without the taxing computational demands of a systematic combinatorial approach.
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