The ontogeny of navigation in Cataglyphis ants

• Applicant: Professor Dr. Wolfgang Rössler
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2018 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 405620408

• Final Report Year: 2023

Final Report Abstract

Cataglyphis desert ants are highly skilled long-distance navigators. Earlier work had shown that experienced Cataglyphis foragers use the position of the sun, particularly associated sky polarization cues, as a compass. The ants integrate this compass input with distance information from a step-integrator to estimate a home vector pointing to the nest along the shortest way possible (path integration). To correct for cumulative errors inherent to path integration, foragers memorize panoramic views, whenever available, as additional guidance cues. The ontogeny of Cataglyphis ants offers an excellent experimental access for studying neuronal mechanisms underlying behavioural development into successful navigators. This project focused on the transition of the ants from performing interior tasks in the dark nest to outdoor foraging in bright sunlight. How is this marked behavioural transition controlled, how do the ants adjust to a new visual environment, and how do the ants learn essential navigational information at the beginning of their foraging careers? We investigated the role of neuropeptides in controlling the interior-exterior transition. Using comprehensive transcriptomic and peptidomic analyses we characterized 71 peptides with likely neuroactive function in Cataglyphis nodus brain; 22 of those were spatially mapped at high resolution using mass spectrometric imaging. Furthermore, we established a 3D atlas of the brain of Cataglyphis nodus comprising 33 neuropils and 30 connecting neuronal fiber tracts as a platform for mapping studies. Changes in mRNA levels of select candidate neuropeptides and associated structural neuronal changes suggest that the neuropeptides corazonin and allatostatin A are involved as modulators during the interior-forager transition. Before heading out on first foraging trips, naïve Cataglyphis ants perform structured learning walks for 2-3 days extending in small loops into different directions close to the entrance of the underground nest. Our manipulation experiments revealed that in contrast to experienced foragers, young ants during learning walks exclusively rely on the Earth’s magnetic field as their reference compass for sampling nest-related panoramic views and calibrating their sky-compass systems. The performance of learning walks leads to plastic changes in visual circuits of integration centers in the mushroom body (MB) calyx and central complex (CX). Rewiring of synaptic boutons from visual projection neurons in the MB calyx and a volume increase in CX circuits require the combined experience of a dynamic (rotating) sky-polarization pattern and a stable magnetic field as a reference compass during learning walks. Based on these results and investigations on sensory projections from visual input and the antennal Johnston’s organ, we develop models how multisensory navigational information is integrated in the ant brain during learning walks.

Publications

• Neuroplasticity in desert ants (Hymenoptera: Formicidae) – importance for the ontogeny of navigation. Myrmecol News 29:1-20.
  Rössler W.
  
• Johnston's organ and its central projections in Cataglyphis desert ants. Journal of Comparative Neurology, 529(8), 2138-2155.
  Grob, Robin; Tritscher, Clara; Grübel, Kornelia; Stigloher, Christian; Groh, Claudia; Fleischmann, Pauline N. & Rössler, Wolfgang
  
• Kompass im Kopf. Biologie in unserer Zeit, 50(2), 100-109.
  Fleischmann, Pauline; Grob, Robin & Rössler, Wolfgang
  
• Magnetoreception in Hymenoptera: importance for navigation. Animal Cognition, 23(6), 1051-1061.
  Fleischmann, Pauline N.; Grob, Robin & Rössler, Wolfgang
  
• The brain of Cataglyphis ants: Neuronal organization and visual projections. Journal of Comparative Neurology, 528(18), 3479-3506.
  Habenstein, Jens; Amini, Emad; Grübel, Kornelia; el Jundi, Basil & Rössler, Wolfgang
  
• Magnetosensation during re-learning walks in desert ants (Cataglyphis nodus). Journal of Comparative Physiology A, 208(1), 125-133.
  Fleischmann, Pauline N.; Grob, Robin & Rössler, Wolfgang
  
• Neuropeptides as potential modulators of behavioral transitions in the ant Cataglyphis nodus. Journal of Comparative Neurology, 529(12), 3155-3170.
  Habenstein, Jens; Thamm, Markus & Rössler, Wolfgang
  
• Sex‐specific and caste‐specific brain adaptations related to spatial orientation in Cataglyphis ants. Journal of Comparative Neurology, 529(18), 3882-3892.
  Grob, Robin; Heinig, Niklas; Grübel, Kornelia; Rössler, Wolfgang & Fleischmann, Pauline N.
  
• Transcriptomic, peptidomic, and mass spectrometry imaging analysis of the brain in the ant Cataglyphis nodus. Journal of Neurochemistry, 158(2), 391-412.
  Habenstein, Jens; Schmitt, Franziska; Liessem, Sander; Ly, Alice; Trede, Dennis; Wegener, Christian; Predel, Reinhard; Rössler, Wolfgang & Neupert, Susanne
  
• Rotation of skylight polarization during learning walks is necessary to trigger neuronal plasticity inCataglyphisants. Proceedings of the Royal Society B: Biological Sciences, 289(1967).
  Grob, Robin; Holland, Cunz Oliver; Grübel, Kornelia; Pfeiffer, Keram; Rössler, Wolfgang & Fleischmann, Pauline N.
  
• The role of learning-walk related multisensory experience in rewiring visual circuits in the desert ant brain. Journal of Comparative Physiology A, 209(4), 605-623.
  Rössler, Wolfgang; Grob, Robin & Fleischmann, Pauline N.