Personality variation in a clonal insect: The pea aphid,<i>Acyrthosiphon pisum</i>

Schuett, Wiebke; Dall, Sasha R. X.; Baeumer, Jana; Kloesener, Michaela H.; Nakagawa, Shinichi; Beinlich, Felix; Eggers, Till

doi:10.1002/dev.20538

Cited by 109 publications

(100 citation statements)

References 64 publications

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“…Genetically identical offspring of the facultatively asexual aphid Acyrthosiphon pisum display surprising variability in their predator avoidance behaviors, a phenomenon that may help the aphid population escape a variety of insectivores (46). Similarly, a quantitative analysis of locomotion in Aphis fabae, another clonal aphid, suggested that individual insects display idiosyncrasy in their food-foraging behaviors (47).…”

Section: Discussionmentioning

confidence: 99%

Neuronal control of locomotor handedness in Drosophila

Buchanan¹,

Kain²,

Bivort

2015

Proc. Natl. Acad. Sci. U.S.A.

144

184

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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...

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Section: Discussionmentioning

confidence: 99%

Neuronal control of locomotor handedness in Drosophila

Buchanan¹,

Kain²,

Bivort

2015

Proc. Natl. Acad. Sci. U.S.A.

144

184

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“…The idiosyncratic behavior of each fly was partially preserved (i.e., dark-preferring flies remained darkpreferring) over at least 4 wk, essentially a fly lifetime. Thus, VBE can be interpreted as phototactic "personality" [sensu (1)]. …”

Section: All Strains Exhibit More Behavioral Variability Than Expectementioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

Phototactic personality in fruit flies and its suppression by serotonin and white

Kain

Stokes

Bivort

2012

Proc. Natl. Acad. Sci. U.S.A.

151

205

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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...

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“…More studies are now desirable that investigate whether behavioral differences induced by developmental effects are consistent and stable, i.e., whether environmental conditions experienced influence animal personalities. Indeed, there is an increasing number of studies focusing on the development of animal personality (e.g., Sinn et al, 2008;Brodin, 2009;Schuett et al, 2011a;Gyuris et al, 2012;Hedrick and Kortet, 2012;Niemelä et al, 2012b;Petelle et al, 2013;Sweeney et al, 2013;Tremmel and Müller, 2013;Guenther et al, 2014;Johnson et al, 2015). To clearly identify underlying processes, experimental studies in which environmental conditions are manipulated are needed.…”

Section: Introductionmentioning

confidence: 99%

Early Environmental Conditions Shape Personality Types in a Jumping Spider

et al. 2015

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Individuals of many species across the animal kingdom are found to be less plastic than expected, even in behavioral traits. The existence of consistent behavioral differences between individuals, termed "personality differences", is puzzling, since plastic behavior is considered ideal to enable animals to adaptively respond to changes in environmental conditions. In order to elucidate which mechanisms are important for the evolution of personality differences, it is crucial to understand which aspects of the environment are important for the development of personality differences. Here, we tested whether physical or social aspects of the environment during development influence individual differentiation (mean level of behavior) using the jumping spider Marpissa muscosa. Furthermore, we assessed whether those behaviors were repeatable, i.e. whether personalities existed. We applied a split-brood design and raised spider siblings in three different environments: a deprived environment with no enrichment, a socially and a physically enriched environment. We focused on exploratory behavior and repeatedly assessed individual behavior in a novel environment and a novel object test. Results show that the environment during development influenced spiders' exploratory tendencies: spiders raised in enriched environments tended to be more exploratory. Most investigated behaviors were repeatable (i.e., personalities existed) across all individuals tested, whereas only few behaviors were also repeatable across individuals that had experienced the same environmental condition. Taken together, our results indicate that external stimuli can influence the development of one aspect of personality, the inter-individual variation (mean level of behavior), in a jumping spider. We also found family by environment interactions on behavioral traits potentially suggesting genetic variation in developmental plasticity.

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Personality variation in a clonal insect: The pea aphid,Acyrthosiphon pisum

Cited by 109 publications

References 64 publications

Neuronal control of locomotor handedness in Drosophila

Neuronal control of locomotor handedness in Drosophila

Phototactic personality in fruit flies and its suppression by serotonin and white

Early Environmental Conditions Shape Personality Types in a Jumping Spider

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