The Subgenual Organ Complex in Stick Insects: Functional Morphology and Mechanical Coupling of a Complex Mechanosensory Organ

Johannes Strauß,Leif Moritz,Peter T Rühr

doi:10.3389/fevo.2021.632493

Abstract

Leg chordotonal organs in insects show different adaptations to detect body movements, substrate vibrations, or airborne sound. In the proximal tibia of stick insects occur two chordotonal organs: the subgenual organ, a highly sensitive vibration receptor organ, and the distal organ, of which the function is yet unknown. The distal organ consists of a linear set of scolopidial sensilla extending in the tibia in distal direction toward the tarsus. Similar organs occur in the elaborate hearing organs in crickets and bushcrickets, where the auditory sensilla are closely associated with thin tympanal membranes and auditory trachea in the leg. Here, we document the position and attachment points for the distal organ in three species of stick insects without auditory adaptations (Ramulus artemis,Sipyloidea sipylus, andCarausius morosus). The distal organ is located in the dorsal hemolymph channel and attaches at the proximal end to the dorsal and posterior leg cuticle by tissue strands. The central part of the distal organ is placed closer to the dorsal cuticle and is suspended by fine tissue strands. The anterior part is clearly separated from the tracheae, while the distal part of the organ is placed over the anterior trachea. The distal organ is not connected to a tendon or muscle, which would indicate a proprioceptive function. The sensilla in the distal organ have dendrites oriented in distal direction in the leg. This morphology does not reveal obvious auditory adaptations as in tympanal organs, while the position in the hemolymph channel and the direction of dendrites indicate responses to forces in longitudinal direction of the leg, likely vibrational stimuli transmitted in the leg’s hemolymph. The evolutionary convergence of complex chordotonal organs with linear sensilla sets between tympanal hearing organs and atympanate organs in stick insects is emphasized by the different functional morphologies and sensory specializations.

Highlights

Structural differentiation in sensory organs commonly correlates to functional specializations (Steinbrecht, 1999; Ridgel et al, 2001; Homberg and Paech, 2002; Land and Nilsson, 2012; Scherberich et al, 2017; Strauß, 2017; Zhao and McBride, 2020)
This is a notable expansion of sensory structures, as the subgenual organ in several insect lineages is the sole chordotonal organ in the proximal tibia and may consist of only few sensilla which are sufficient for detection of vibration signals (Michel et al, 1982; Nishino et al, 2016; Cokl et al, 2019)
The subgenual organ complex in stick insects consists of the subgenual organ (SGO) and the distal organ (DO), and the latter has a notable linear organization of sensilla (Strauß and Lakes-Harlan, 2013)

Summary

INTRODUCTION

Structural differentiation in sensory organs commonly correlates to functional specializations (Steinbrecht, 1999; Ridgel et al, 2001; Homberg and Paech, 2002; Land and Nilsson, 2012; Scherberich et al, 2017; Strauß, 2017; Zhao and McBride, 2020). Sub-groups of sensilla or several organs occur in close proximity (Field and Matheson, 1998) For the latter, the subgenual organ complex in orthopteroid insects provides an example of 2–4 chordotonal organs located in the leg (Strauß et al, 2014). For insect chordotonal organs, which repeatedly evolved a complex structure or a high number of sensory neurons (Field and Matheson, 1998; Yack, 2004), the functional morphology can indicate their physiological role by identifying how sensilla are stimulated by mechanical energy from their coupling to different structures like cuticle or tracheae. Understanding the functional morphology of the DO of stick insects in more detail will give insights into the extent of evolutionary convergence in the DO to the auditory sensilla in crickets and tettigoniids

MATERIALS AND METHODS

RESULTS

DISCUSSION