Co-option of a motor-to-sensory histaminergic circuit correlates with insect flight biomechanics.

Phillip D Chapman,Kassandra E Riggs,Kevin C Daly,Erica J Haught,Mouaz M Haffar,Samual P Bradley,Andrew M Dacks

doi:10.1098/rspb.2017.0339

Phillip D Chapman, Kassandra E Riggs + Show 5 more

Open Access

https://doi.org/10.1098/rspb.2017.0339

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Abstract

Nervous systems must adapt to shifts in behavioural ecology. One form of adaptation is neural exaptation, in which neural circuits are co-opted to perform additional novel functions. Here, we describe the co-option of a motor-to-somatosensory circuit into an olfactory network. Many moths beat their wings during odour-tracking, whether walking or flying, causing strong oscillations of airflow around the antennae, altering odour plume structure. This self-induced sensory stimulation could impose selective pressures that influence neural circuit evolution, specifically fostering the emergence of corollary discharge circuits. In Manduca sexta, a pair of mesothoracic to deutocerebral histaminergic neurons (MDHns), project from the mesothoracic neuromere to both antennal lobes (ALs), the first olfactory neuropil. Consistent with a hypothetical role in providing the olfactory system with a corollary discharge, we demonstrate that the MDHns innervate the ALs of advanced and basal moths, but not butterflies, which differ in wing beat and flight pattern. The MDHns probably arose in crustaceans and in many arthropods innervate mechanosensory areas, but not the olfactory system. The MDHns, therefore, represent an example of architectural exaptation, in which neurons that provide motor output information to mechanosensory regions have been co-opted to provide information to the olfactory system in moths.

Highlights

Exaptation is a core feature in the development of new phenotypic traits, allowing pre-existing traits to be co-opted to take on new or additional roles
There are 11 pairs of histaminergic neurons in the brain of M. sexta [15], ablation experiments have demonstrated that the mesothoracic to deutocerebral histaminergic neurons (MDHns) are the sole source of histamine in the antennal lobes (ALs) [13]
In the AL of M. sexta, the HisClB receptor is expressed by a subset of GABAergic local interneurons that innervate every glomerulus [13], and histamine immunoreactivity (HA-ir) itself is constrained to several ventral glomeruli, this it is likely that the MDHns provide fast inhibitory input to a subset of neurons that themselves exert network-wide inhibition

Summary

Introduction

Exaptation is a core feature in the development of new phenotypic traits, allowing pre-existing traits to be co-opted to take on new or additional roles. The MDHns branch extensively within the mesothoracic neuromere (MsN) and project ascending axons to innervate the suboesophageal zone (SEZ), antennal mechanosensory and motor centre (AMMC) and antennal lobe (AL) [13,15] (figure 1a). There are 11 pairs of histaminergic neurons in the brain of M. sexta [15], ablation experiments have demonstrated that the MDHns are the sole source of histamine in the AL [13].

Results

Conclusion