Neuropeptides as potential modulators of behavioral transitions in the ant Cataglyphis nodus

Abstract

Age‐related behavioral plasticity is a major prerequisite for the ecological success of insect societies. Although ecological aspects of behavioral flexibility have been targeted in many studies, the underlying intrinsic mechanisms controlling the diverse changes in behavior along the individual life history of social insects are not completely understood. Recently, the neuropeptides allatostatin‐A, corazonin, and tachykinin have been associated with the regulation of behavioral transitions in social insects. Here, we investigated changes in brain localization and expression of these neuropeptides following major behavioral transitions in Cataglyphis nodus ants. Our immunohistochemical analyses in the brain revealed that the overall branching pattern of neurons immunoreactive (ir) for the three neuropeptides is largely independent of the behavioral stages. Numerous allatostatin‐A‐ and tachykinin‐ir neurons innervate primary sensory neuropils and high‐order integration centers of the brain. In contrast, the number of corazonergic neurons is restricted to only four neurons per brain hemisphere with cell bodies located in the pars lateralis and axons extending to the medial protocerebrum and the retrocerebral complex. Most interestingly, the cell‐body volumes of these neurons are significantly increased in foragers compared to freshly eclosed ants and interior workers. Quantification of mRNA expression levels revealed a stage‐related change in the expression of allatostatin‐A and corazonin mRNA in the brain. Given the presence of the neuropeptides in major control centers of the brain and the neurohemal organs, these mRNA‐changes strongly suggest an important modulatory role of both neuropeptides in the behavioral maturation of Cataglyphis ants.

Magnetosensation during re-learning walks in desert ants (Cataglyphis nodus)

“…The ant brain, particularly synaptic relay stations in high-order integration centers along two visual pathways, undergoes plastic changes during the iLW phase (Grob et al 2017 , 2019 ; Rössler 2019 ; Stieb et al 2012 ). Furthermore, the transition from interior to exterior worker is accompanied by changes in the expression levels of neuropeptides playing an important role in behavior control (Habenstein et al 2021 ). This neuroplasticity supports the fact that novices perform visual learning and calibrate their visual guidance systems to acquire all information for orientation during foraging, e.g.…”

“…Cataglyphis ants use up to 3 days to perform learning walks (LWs) to acquire all information for orientation during foraging far away from the nest (Fleischmann et al 2016 , 2018b ; Stieb et al 2012 ; Wehner et al 2004 ; for a review: Zeil and Fleischmann 2019 ). The transition from interior to exterior worker is not only characterized by changes in behavior, but also leads to neuroplastic changes along visual pathways in the ant brain (Grob et al 2017 ; Habenstein et al 2021 ; Schmitt et al 2016 ; Stieb et al 2012 ; for reviews: Grob et al 2019 ; Rössler 2019 ). The iLWs include pirouettes, rotational body movements that are full or partial turns during which the novices stop several times (Fleischmann et al 2017 ).…”

The role of learning-walk related multisensory experience in rewiring visual circuits in the desert ant brain

“…In addition to the neuroanatomical studies, analyses of neuropeptides and their localization in the Cataglyphis brain have recently been performed. For this, transcriptomal analyses were combined with mass spectrometry detection and localization to reveal the most comprehensive neuropeptidome that has been obtained from an ant's brain so far (Habenstein et al 2021a(Habenstein et al , 2021bSchmitt et al 2017). Both the neuroanatomical and neuropeptidome databases provide rich sources for future structure-function analyses in the brain of Cataglyphis ants, for example, to detect life-stage dependent changes in brain neuropils and neuromodulators, and for comparison of those attributes with other ant species.…”

Insecticidal efficacy and risk assessment of different neuropeptide analog combinations against the peach‐potato aphid following topical exposure

“…[22][23] More recently, evidence has also been reported that TRPs modulate both olfactory sensitivity and locomotor activity. 24,25 The insect MS neuropeptide inhibits visceral muscle contractions, while stimulating skeletal muscle contraction and enzyme secretion from digestive tissue. 26 In cockroaches, MS inhibits contractions of the foregut and hindgut.…”

“…TRPs have been shown to stimulate Malpighian tubules writhing in the locust Locusta migratoria , and stimulate diuretic activity in tubules of the locust Schistocerca gregaria 22–23 . More recently, evidence has also been reported that TRPs modulate both olfactory sensitivity and locomotor activity 24,25 . The insect MS neuropeptide inhibits visceral muscle contractions, while stimulating skeletal muscle contraction and enzyme secretion from digestive tissue 26 .…”