Developmental constraint of insect audition

Abstract

Background: Insect ears contain very different numbers of sensory cells, from only one sensory cell in some moths to thousands of sensory cells, e.g. in cicadas. These differences still await functional explanation and especially the large numbers in cicadas remain puzzling. Insects of the different orders have distinct developmental sequences for the generation of auditory organs. These sensory cells might have different functions depending on the developmental stages. Here we propose that constraints arising during development are also important for the design of insect ears and might influence cell numbers of the adults.

Presentation of the hypothesis: We propose that the functional requirements of the subadult stages determine the adult complement of sensory units in the auditory system of cicadas. The hypothetical larval sensory organ should function as a vibration receiver, representing a functional caenogenesis.

Testing the hypothesis: Experiments at different levels have to be designed to test the hypothesis. Firstly, the neuroanatomy of the larval sense organ should be analyzed to detail. Secondly, the function should be unraveled neurophysiologically and behaviorally. Thirdly, the persistence of the sensory cells and the rebuilding of the sensory organ to the adult should be investigated.

Implications of the hypothesis: Usually, the evolution of insect ears is viewed with respect to physiological and neuronal mechanisms of sound perception. This view should be extended to the development of sense organs. Functional requirements during postembryonic development may act as constraints for the evolution of adult organs, as exemplified with the auditory system of cicadas.

Figure 1

Outline of the developmental schemes for audition in six orders of insects. In the two taxa Coleoptera and Diptera of holometabolous insects the scolopidial sense organ for hearing develops during the pupal stage (generation of cells: yellow; differentiation: dotted line). Shortly after emergence the adult hearing capability is aquired (red). In at least some Lepidoptera the scolopidia develop during embryogenesis and are remodeled during the pupal stage (broken line) for the innervation of the adult tympanal organ. The larval function is probably proprioception (blue). In the Hemimetabola the scolopidia are formed during embryogenesis. In the Saltatoria and the Mantodea, the hearing capabilities develop gradually with the postembryonic larval stages (blue-red line). In the Auchenorrhyncha the cells probably develop during embryogensis and two separate functions are proposed for the larva and the adult (see text).