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

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.

Keywords: arthropod; evolution; exaptation; histamine; olfaction.

Figure 1.

MDHns in macrolepidopteran moths innervate the ALs. (a) Schematic of MDHns (green) in M. sexta. Each MDHn innervates the SEZ and AMMC before projecting to both ALs. (b) Whole-mount M. sexta pterothoracic ganglion immunolabelled for HA. MDHns are the most anterior pair of histaminergic neurons (arrow heads). Depth: 166.6 µm. (c) Frontal section of M. sexta AL immunolabelled for HA (green). Bruchpilot immunolabelling delineates neuropil (magenta). Depth: 52.36 µm. (d) Sagittal section of B. mori MsN immunolabelled for HA. Depth: 133 µm. (e) Sagittal section of B. mori AL immunolabelled for HA (green). Bruchpilot immunolabelling delineates neuropil (magenta). Depth: 58.8 µm. (f) Whole-mount sagittal view of I. aemula pterothoracic ganglion. Depth: 164.64 µm. (g) Sagittal section of I. aemula AL immunolabelled for HA (green). Bruchpilot immunolabelling delineates neuropil (magenta). Bruchpilot (magenta) is used to delineate neuropil. HA-ir (green). Depth: 124 µm. Scale bars, 100 µm. Arrows, cell bodies; arrow heads, ascending axons; hatched white lines in (e) and (g) delineates the boundary of the AL.

Figure 2.

MDHns do not innervate ALs in butterflies. (a) Full central nervous system montage of HA-ir in P. rapae. Depth: 239.86 µm. (b) Whole-mount sagittal view of P. rapae MsN. Depth: 157.36 µm. (c) P. rapae AL showing absence of HA-ir (green). Bruchpilot immunolabelling delineates neuropil (magenta). Depth: 29.68 µm. (d) Whole-mount frontal view of L. archippus of brain showing no AL HA-ir. HA-ir can be seen directly posterior of the left AL in (d) (depth: 39.38 µm) however optical stacks restricted to the depth of tissue including only the AL (depth: 21.48 µm) demonstrate that these HA-ir processes do not enter the AL. (e) Horizontal view of MsN of P. appalachiensis. Depth: 170.05 µm. (f) Horizontal section of P. appalachiensis brain showing no HA-ir (green) in the AL. Bruchpilot (magenta) delineates neuropil. Depth: 25.76 µm. Scale bars, 100 µm. Arrows, cell bodies; arrow heads, ascending axons; hatched white lines in (c,d,f) delineates the boundary of the AL.

Figure 3.

The MDHns in Microlepidoptera and Trichoptera innervate the ALs. (a) Whole-mount horizontal view of G. mellonella MsN. Depth: 123.3 µm. (b) Whole-mount frontal view of G. mellonella brain showing HA-ir (green) in the AL. Bruchpilot (magenta) delineates neuropil. Depth: 46.77 µm. (c) Whole-mount horizontal view of G. molesta MsN. Depth: 147.11 µm. (d) Whole-mount frontal view of G. molesta brain. Depth: 40.8 µm. (d) Whole-mount horizontal view of caddisfly (Limnephilidae) MsN. Depth: 103.82 µm. (f) Whole-mount frontal view of caddisfly (Limnephilidae) brain showing HA-ir (green) processes within the AL (brackets). Bruchpilot (magenta) delineates neuropil. Depth: 144.99 µm. Scale bars, 100 µm. Arrows, cell bodies; arrow heads, ascending axons; hatched white lines in (b,d,f) delineates the boundary of the AL.

Figure 4.

MDHns are present in the majority of arthropods. (a) Whole-mount horizontal view of the ventral nervous system of D. melanogaster. Depth: 132 µm. (b) Whole-mount frontal view of the brain of D. melanogaster. No HA-ir is observed in the ALs (insets). Bruchpilot (magenta) delineates neuropil. Depth: 132 µm. (c) Whole-mount horizontal view of the MsN of T. molitor immunolabelled for HA. Depth: 156 µm. (d) Whole-mount horizontal view of thoracic ganglia of O. fasciatus immunolabelled for HA. Depth: 211.22 µm. (e) Whole-mount horizontal view of the MsN of G. lurida immunolabelled for HA. Depth: 140 µm. (f) Whole-mount horizontal view of the first post-cephalic ganglion in T. californiensis immunolabelled for HA. Depth: 97.29 µm. (g) Whole-mount horizontal view of the synganglion in A. americanum. Depth: 119 µm. Scale bars, 100 µm. Arrows, cell bodies; arrow heads, ascending axons; hatched white lines in (b) delineates the boundary of the AL.

Figure 5.

Schematic representation of the proposed evolutionary history of the MDHns. In this representation, the MDHns originally projected from the mesothoracic neuromere (MsN, blue) to the sub-oesophageal zone and antennal mechanosensory and motor centre (AMMC/SEZ, lavender). In the last common ancestor of the Lepidoptera and Trichoptera, the MDHns were co-opted (1; Dashed MDHn branches) to innervate the antennal lobes (ALs, magenta). The innervation of the ALs was lost in the butterflies (2), but maintained in macrolepidoteran moths.