Abstract
Innate behavioral biases such as human handedness are a ubiquitous form of inter-individual variation that are not strictly hardwired into the genome and are influenced by diverse internal and external cues. Yet, genetic and environmental factors modulating behavioral variation remain poorly understood, especially in vertebrates. To identify genetic and environmental factors that influence behavioral variation, we take advantage of larval zebrafish light-search behavior. During light-search, individuals preferentially turn in leftward or rightward loops, in which directional bias is sustained and non-heritable. Our previous work has shown that bias is maintained by a habenula-rostral PT circuit and genes associated with Notch signaling. Here we use a medium-throughput recording strategy and unbiased analysis to show that significant individual to individual variation exists in wildtype larval zebrafish turning preference. We classify stable left, right, and unbiased turning types, with most individuals exhibiting a directional preference. We show unbiased behavior is not due to a loss of photo-responsiveness but reduced persistence in same-direction turning. Raising larvae at elevated temperature selectively reduces the leftward turning type and impacts rostral PT neurons, specifically. Exposure to conspecifics, variable salinity, environmental enrichment, and physical disturbance does not significantly impact inter-individual turning bias. Pharmacological manipulation of Notch signaling disrupts habenula development and turn bias individuality in a dose dependent manner, establishing a direct role of Notch signaling. Last, a mutant allele of a known Notch pathway affecter gene, gsx2, disrupts turn bias individuality, implicating that brain regions independent of the previously established habenula-rostral PT likely contribute to inter-individual variation. These results establish that larval zebrafish is a powerful vertebrate model for inter-individual variation with established neural targets showing sensitivity to specific environmental and gene signaling disruptions. Our results provide new insight into how variation is generated in the vertebrate nervous system.
Highlights
Inter-individual variation, or individuality, is a hallmark of most animal species and contributes to the population’s fitness and ability to adapt when confronted with environmental change (Dingemanse et al, 2004; Klein et al, 2017; Horváth et al, 2020)
We developed a multiplexed strategy to record path trajectories to assess inter-individual variation during larval zebrafish light search behavior (Figure 1A)
We reveal that during light-search initiated by the loss of illumination, larval zebrafish exhibit significant inter-individual variation in turn bias, a handed-like behavior
Summary
Inter-individual variation, or individuality, is a hallmark of most animal species and contributes to the population’s fitness and ability to adapt when confronted with environmental change (Dingemanse et al, 2004; Klein et al, 2017; Horváth et al, 2020). One form of inter-individual variation is sensory and motor biases. Handedness in humans is a familiar example, expressed as a sustained preference for left- or right-hand use, which the expression of a specific hand preference is only partially explained by genetics, suggesting complex interactions contribute to imposing handed phenotypes (Cuellar-Partida et al, 2020). Handed biases are a conserved form of individual behavioral variation with species as diverse as hagfish (Miyashita and Palmer, 2014), Drosophila (Kain et al, 2012; Buchanan et al, 2015), chicken (Rogers, 1982; Casey and Karpinski, 1999), and various vertebrate paw/foot biases (Bulman-Fleming et al, 1997; Brown and Magat, 2011; Giljov et al, 2013; Schiffner and Srinivasan, 2013; Manns et al, 2021) showing sustained individual motor preferences. Despite the prevalence of handed behaviors, mechanisms instructing these behaviors and the variation observed across individuals are still poorly understood
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