Abstract

BackgroundInsect 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 hypothesisWe 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 hypothesisExperiments 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 hypothesisUsually, 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.

Highlights

  • 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

  • Tympanal hearing in insects evolved more than 10 times independently from each other [1,2,3]. These tympanal organs are located at different sites on the insect body and have distinct designs, but with common features, like a scolopidial sense organ. These sense organs belong to a family of internal mechanoreceptors found in arthropods

  • Phylogenetic comparison revealed that scolopidial sense organs are in the same place in hearing and non-hearing species, while hearing species having external structures elaborated for perception of airborne sound [4,5]

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Summary

Background

Insect audition represents a fascinating example of multiple evolution in several lineages. The hypothesis presented here postulates the functional need of a vibration receptor with a high number of sensory units in larval stages of cicadas, which are retained into the adult and become transformed into an auditory system sensitive to airborne sound. We direct the perspective away from the adult system and look at ontogenetic factors which can influence the design of an insect ear This is a refocus of research questions, the life cycles of many insects are not as complex as the cicada's and caenogenesis in auditory structures might not be the rule. The embryonic development could be necessary when restrictions in the genetic mechanisms require that sensory mother cells occur only in the embryo, but not during postembryonic stages This perspective forces one to carefully discriminate between primary and secondary adaptations in a studied system. Functional requirements during development may http://www.frontiersinzoology.com/content/3/1/20 act as constraints for the evolution of adult organs, as exemplified with the auditory system of cicadas

Yager DD
Boyan GS
10. Stumpner A
12. Pollack GS
16. Römer H
18. Laughlin SB
23. Klose M
28. Gould SJ
34. Minelli A
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