A projectome of the bumblebee central complex

Elife. 2021 Sep 15:10:e68911. doi: 10.7554/eLife.68911.

Abstract

Insects have evolved diverse and remarkable strategies for navigating in various ecologies all over the world. Regardless of species, insects share the presence of a group of morphologically conserved neuropils known collectively as the central complex (CX). The CX is a navigational center, involved in sensory integration and coordinated motor activity. Despite the fact that our understanding of navigational behavior comes predominantly from ants and bees, most of what we know about the underlying neural circuitry of such behavior comes from work in fruit flies. Here, we aim to close this gap, by providing the first comprehensive map of all major columnar neurons and their projection patterns in the CX of a bee. We find numerous components of the circuit that appear to be highly conserved between the fly and the bee, but also highlight several key differences which are likely to have important functional ramifications.

Keywords: bombus terrestris; central complex; electron microscopy; insects; navigation; neuroanatomy; neuroscience.

Plain language summary

Bumblebees forage widely for pollen and nectar from flowers, sometimes travelling kilometers away from their nest, but they can somehow always find their way home in a nearly straight line. These insects have been known to return to their nest from new locations almost 10 kilometers away. This homing ability is a complex neurological feat and requires the brain to combine several processes, including observing the external world, controlling bodily movements and drawing on memory. While the navigational behavior of bees has been well-studied, the neuronal circuitry behind it has not. Unfortunately, most of what is known about insects’ brain activity comes from studies in species such as locusts or fruit flies. In these species, a region of the brain known as the central complex has been shown to have an essential role in homing behaviors. However, it is unknown how similar the central complex of bumblebees might be to fruit flies’ or locusts’, or how these differences may affect navigational abilities. Sayre et al. obtained images of thin slices of the bumblebee central complex using a technique called block-face electron microscopy, which produces high-resolution image volumes. These images were used to obtain a three-dimensional map of over 1300 neurons. This cellular atlas showed that key aspects of the central complex are nearly identical between flies and bumblebees, including the internal compass that monitors what direction the insect is travelling in. However, hundreds of millions of years of independent evolution have resulted in some differences. These were found in neurons possibly involved in forming memories of the directions and lengths of travelled paths, and in the circuits that use such vector memories to steer the insects towards their targets. Sayre et al. propose that these changes underlie bees’ impressive ability to navigate. These results help explain how the structure of insects’ brains can determine homing abilities. The insights gained could be used to develop efficient autonomous navigation systems, which are challenging to build and require a lot more processing power than offered by a small part of an insect brain.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Bees / physiology*
  • Bees / ultrastructure
  • Behavior, Animal*
  • Connectome*
  • Drosophila melanogaster / physiology
  • Drosophila melanogaster / ultrastructure
  • Flight, Animal*
  • Neural Pathways / physiology*
  • Neural Pathways / ultrastructure
  • Neuropil / physiology*
  • Neuropil / ultrastructure
  • Spatial Behavior*
  • Species Specificity

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.