Bold Behavior Is Associated with Genes That Regulate Energy Use but Does Not Covary with Body Condition in Food-Restricted Snails.

Abstract

Theoretical models about the relationship between food restriction and individual differences in risk-taking behavior (i.e., boldness) have led to conflicting predictions: some models predict that food restriction increases boldness, while other models predict that food restriction decreases boldness. This discrepancy may be partially attributable to an underappreciation for animals’ complex physiological responses to food restriction. To understand the proximate mechanisms mediating state-dependent boldness, we used freshwater snails (Helisoma trivolvis) to examine the relationships among food availability, body condition, boldness (latency to reemerge from shell and exploration), and mRNA expression of three genes (adenosine monophosphate–activated protein kinase [AMPK], molluscan insulin-like peptide [MIP], and serotonin receptor [5-HT]) involved in maintaining energy homeostasis during periods of moderate food restriction. Latency to reemerge and exploratory behavior decreased over time, but fed snails were bolder than fasted snails, suggesting that food restriction reduces bold behavior. Although food restriction decreased body condition, there was not a relationship between body condition and latency to reemerge from shell. However, expression of MIP was positively correlated with latency to reemerge from shell. Furthermore, AMPK was positively correlated with MIP and negatively correlated with body condition and 5-HT. Therefore, individual differences in physiological responses to food restriction, not overall body condition per se, appear to be more closely associated with state-dependent bold behavior. Finally, snails that experienced a novel assay environment returned to their initial “shy” behavior, suggesting that habituation to the assay environment may contribute to snails expressing bolder behavior over time.