Forager age and foraging state, but not cumulative foraging activity, affect biogenic amine receptor gene expression in the honeybee mushroom bodies

Abstract

Foraging behavior is crucial for the development of a honeybee colony. Biogenic amines are key mediators of learning and the transition from in‐hive tasks to foraging. Foragers vary considerably in their behavior, but whether and how this behavioral diversity depends on biogenic amines is not yet well understood. For example, forager age, cumulative foraging activity or foraging state may all be linked to biogenic amine signaling. Furthermore, expression levels may fluctuate depending on daytime. We tested if these intrinsic and extrinsic factors are linked to biogenic amine signaling by quantifying the expression of octopamine, dopamine and tyramine receptor genes in the mushroom bodies, important tissues for learning and memory. We found that older foragers had a significantly higher expression of Amdop1, Amdop2, AmoctαR1, and AmoctβR1 compared to younger foragers, whereas Amtar1 showed the opposite pattern. Surprisingly, our measures of cumulative foraging activity were not related to the expression of the same receptor genes in the mushroom bodies. Furthermore, we trained foragers to collect sucrose solution at a specific time of day and tested if the foraging state of time‐trained foragers affected receptor gene expression. Bees engaged in foraging had a higher expression of Amdop1 and AmoctβR3/4 than inactive foragers. Finally, the expression of Amdop1, Amdop3, AmoctαR1, and Amtar1 also varied with daytime. Our results show that receptor gene expression in forager mushroom bodies is complex and depends on both intrinsic and extrinsic factors.

The Insect Type 1 Tyramine Receptors: From Structure to Behavior

“…In contrast, OAR1 exhibited the opposite expression profile [70]. Therefore, it can be proposed that, in social insects, TAR1 could represent a key element in defining the caste identity and modulating behavioral features such as olfaction [71]. Behavioral alterations caused by TAR1 modulation have been observed in several studies performed with L. migratoria and D. melanogaster.…”

Octopamine affects gustatory responsiveness and associative learning performance in bumble bees

“…OA receptor expression in the brains of nurses vs. foragers differs (Reim and Scheiner, 2014; Schulz and Robinson, 2001), as do OA titers (Schulz et al, 2002). Among foragers, patterns of OA receptor expression change with age (Peng et al, 2021) and OA-mediated differences may underlie individual-level patterns of resource specialization (Arenas et al, 2021; Giray et al, 2007). For example, OA’s influence on sucrose response thresholds determines the quality of food they bring back when foraging (Giray et al, 2007; Pankiw and Page Jr., 1999).…”

Use of waggle dance information in honey bees is linked to gene expression in the antennae, but not in the brain

“…Social insect behaviour and, in particular, foraging strategies are linked to gene expression in the brain (Ingram et al, 2011; Robinson et al, 2008; Toth & Robinson, 2009; Toth et al, 2010; Zayed & Robinson, 2012). Behavioural variation among workers and within foragers seems to be strongly connected to biogenic amine signalling, such as dopamine, octopamine, tyramine, and serotonin signalling (Arenas et al, 2020; Barron et al, 2002; Liang et al, 2012; Linn et al, 2020; Mercer & Menzel, 1982; Peng et al, 2020, 2021; Scheiner et al, 2002, 2017; Schulz et al, 2003). Transcriptomic differences between behavioural groups were typically studied by investigating the entire brain (e.g., Alleman et al, 2019; Liang et al, 2012; Whitfield et al, 2003).…”