A neurodevelopmental origin of behavioral individuality in the
            <i>Drosophila</i>
            visual system

Linneweber, Gerit Arne; Andriatsilavo, Maheva; Dutta, Suchetana; Bengochea, Mercedes; Hellbruegge, Liz; Liu, Guangda; Ejsmont, Radoslaw K; Straw, Andrew; Wernet, Mathias F.; Hiesinger, P. Robin; Hassan, Bassem A.

doi:10.1126/science.aaw7182

Cited by 126 publications

(161 citation statements)

References 62 publications

(100 reference statements)

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“…We expect that individuals from a bet-hedging genotype would exhibit stable idiosyncratic behavioral biases when reared in the same environment. Isogenic Drosophila melanogaster, reared in a constant lab environment, exhibit consistent, but widely varying, individual behaviors -examples include turning bias [27][28][29] , phototaxis 30 , thermal preference 12 , and odor preference 31 . These differences are termed intragenotypic variability, and they may reflect a bet-hedging strategy.…”

Section: Introductionmentioning

confidence: 99%

Wild flies hedge their thermal preference bets in response to seasonal fluctuations

Akhund-Zade

Yoon

Bangerter

et al. 2020

Preprint

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Fluctuating environmental pressures can challenge organisms by repeatedly shifting the optimum phenotype. Two contrasting evolutionary strategies to cope with these fluctuations are 1) evolution of the mean phenotype to follow the optimum (adaptive tracking) or 2) diversifying phenotypes so that at least some individuals have high fitness in the current fluctuation (bet-hedging). Bet-hedging could underlie stable differences in the behavior of individuals that are present even when genotype and environment are held constant. Instead of being simply ‘noise,’ behavioral variation across individuals may reflect an evolutionary strategy of phenotype diversification. Using geographically diverse wild-derived fly strains and high-throughput assays of individual preference, we tested whether thermal preference variation in Drosophila melanogaster could reflect a bet-hedging strategy. We also looked for evidence that populations from different regions differentially adopt bet-hedging or adaptive-tracking strategies. Computational modeling predicted regional differences in the relative advantage of bet-hedging, and we found patterns consistent with that in regional variation in thermal preference heritability. In addition, we found that temporal patterns in mean preference support bet-hedging predictions and that there is a genetic basis for thermal preference variability. Our empirical results point to bet-hedging in thermal preference as a potentially important evolutionary strategy in wild populations.

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Section: Introductionmentioning

confidence: 99%

Wild flies hedge their thermal preference bets in response to seasonal fluctuations

Akhund-Zade

Yoon

Bangerter

et al. 2020

Preprint

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“…We have edited the genomic locus of the to detect FoxP expression) had no effect in Buridan's paradigm (Fig. 9), despite these neurons being required for normal locomotion in Buridan's paradigm (Linneweber et al, 2020;Serway et al, 2009;Xiong et al, 2010). In contrast, without FoxP in the protocerebral bridge or motor neurons, flies show similar locomotor impairments as flies with constitutive knockouts (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…In both experiments, the effects of the manipulations were so severe, that it was not possible to reach the target sample size of 18. Recently, Linneweber et al (2020) described the consequences of silencing dorsal cluster neurons (DCNs) on stripe fixation behavior in Buridan's paradigm. The FoxP-iB expression pattern suggests that at least some of these DCNs express FoxP (Fig.…”

Section: Foxp-ib Expression In the Drosophila Brainmentioning

confidence: 99%

“…The only case where only one set of parameters was affected were the FoxP 3955 mutant flies (Fig. 6) MBs have been shown to affect both spatial and temporal aspects of locomotion (Besson and Martin, 2005;Helfrich-Förster et al, 2002;Lark et al, 2017;Lebreton and Martin, 2009;Mabuchi et al, 2016;Manjila et al, 2019; e.g., Martin et al, 1998;Serway et al, 2009;Sun et al, 2018;Xiong et al, 2010) (Linneweber et al, 2020), but removing FoxP from DCNs showed no effect (Fig. 9B), despite abundant FoxP expression in DCNs (Fig.…”

Section: Foxp Expressionmentioning

confidence: 99%

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Identification ofFoxPcircuits involved in locomotion and object fixation inDrosophila

Palazzo

Rass

Brembs

2020

Preprint

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The FoxP family of transcription factors is necessary for operant self-learning, an evolutionary conserved form of motor learning. The expression pattern, molecular function and mechanisms of action of the Drosophila FoxP orthologue remain to be elucidated. By editing the genomic locus of FoxP with CRISPR/Cas9, we find that the three different FoxP isoforms are expressed in neurons, but not in glia and that not all neurons express all isoforms. Furthermore, we detect FoxP expression in, e.g., the protocerebral bridge, the fan shaped body and in motorneurons, but not in the mushroom bodies. Finally, we discover that FoxP expression during development, but not adulthood, is required for normal locomotion and landmark fixation in walking flies. While FoxP expression in the protocerebral bridge and motorneurons is involved in locomotion and landmark fixation, the FoxP gene can be deleted from dorsal cluster neurons and mushroom-body Kenyon cells without affecting these behaviors.

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“…Variability also encompasses individuality in animal behavior, typically defined as a trait-like feature that persists stably over several observations. Individuality has been identified in fruit fly turning decisions (21), mouse roaming behavior (22), and bumblebee foraging behavior (23), among others (24,25), indicating the importance of considering within-individual variability, or the degree to which an individual's behavior varies in repeated trials. Our analysis found no evidence for individuality in grooming, as Canton-S flies exhibited similar degrees of within-individual variability and between-individual variation.…”

Section: Genetic Influences Of Behavioral Variation and Variabilitymentioning

confidence: 99%

Variation and variability in Drosophila grooming behavior

Mueller¹,

Zhang

Carlson³

et al. 2020

Preprint

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Behavioral differences can be observed between species or populations (variation) or between individuals in a genetically similar population (variability). Here, we investigate genetic differences as a possible source of variation and variability in Drosophila grooming. Drosophila grooming behavior confers survival and social benefits. Although the leg movements that constitute the grooming sequence are stereotyped, their order is not fixed. Grooming features of five drosophilid species exposed to a dust irritant were analyzed. Components of grooming behavior were conserved between and within species. However, significant differences in grooming syntax were identified, corresponding both to anterior and posterior grooming actions. Genetic heterogeneity was not found to be related to grooming variability, as melanogaster flies bred to increase genetic heterogeneity did not exhibit increased variability in grooming syntax. Likewise, no relationship between decreased heterogeneity and variability was identified. Finally, individual melanogaster flies were observed on consecutive days to determine the degree of variability of grooming behavior within an individual over time. Individual flies were not found to possess strong, stable grooming traits over several recordings. Additionally, standardization of sensory input using optogenetics did not eliminate grooming variability. In aggregate, these data suggest the importance of sensory inputs and other factors such as life history in grooming variability.

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A neurodevelopmental origin of behavioral individuality in the Drosophila visual system

Cited by 126 publications

References 62 publications

Wild flies hedge their thermal preference bets in response to seasonal fluctuations

Wild flies hedge their thermal preference bets in response to seasonal fluctuations

Identification ofFoxPcircuits involved in locomotion and object fixation inDrosophila

Variation and variability in Drosophila grooming behavior

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