Sensory evolution of hearing in tettigoniids with differing communication systems

Abstract

In Tettigoniidae (Orthoptera: Ensifera), hearing organs are essential in mate detection. Male tettigoniids usually produce calling songs by tegminal stridulation, whereas females approach the males phonotactically. This unidirectional communication system is the most common one among tettigoniids. In several tettigoniid lineages, females have evolved acoustic replies to the male calling song which constitutes a bidirectional communication system. The genus Poecilimon (Tettigoniidae: Phaneropterinae) is of special interest because the ancestral state of bidirectional communication, with calling males and responding females, has been reversed repeatedly to unidirectional communication. Acoustic communication is mediated by hearing organs that are adapted to the conspecific signals. Therefore, we analyse the auditory system in the Tettigoniidae genus Poecilimon for functional adaptations in three characteristics: (i) dimension of sound-receiving structures (tympanum and acoustic spiracle), (ii) number of auditory sensilla and (iii) hearing sensitivity. Profound differences in the auditory system correlate with uni-or bidirectional communication. Among the sound-receiving structures, the tympana scale with body size, whereas the acoustic spiracle, the major sound input structure, was drastically reduced in unidirectional communicating species. In the unidirectional P. ampliatus group, auditory sensilla are severely reduced in numbers, but not in the unidirectional P. propinquus group. Within the P. ampliatus group, the number of auditory sensilla is further reduced in P. intermedius which lost acoustic signalling due to parthenogenesis. The auditory sensitivity correlated with the size of the acoustic spiracle, as hearing sensitivity was better with larger spiracles, especially in the ultrasonic range. Our results show a significant reduction in auditory structures, shaped by the differing sex roles during mate detection.

Selective forces on origin, adaptation and reduction of tympanal ears in insects

“…Also in the groups of P. ampliatus/P. propinquus there are species with unidirectional and bidirectional communication systems between females and males; the bidirectional species has larger spiracles (potentially because females produce the softer songs) and, therefore, the communication system may pose additional selective forces on hearing leading to the same differences in ear morphology as under the selective forces described above (Strauß et al 2014a; see below).…”

“…Evidently, evolutionary reduction in Orthoptera affects the tympana to a greater extent than auditory sensory neurons (Lakes-Harlan et al 1991;Lehmann et al 2010). Yet, in some Poecilimon tettigoniids, neuron numbers may also decrease considerably while tympana and hearing are maintained (Strauß et al 2014a). However, rigorous case studies of reduction across insects are few so far.…”

“…Nevertheless, within the European tettigoniid genus Poecilimon, neuronal regression was found following the loss of complex acoustic duets between sexes. Members of one such lineage have a smaller number of auditory sensilla compared to outgroup species as well as to species which represent the ancestral signalling mode (Strauß et al 2014a). However, across different insect taxa, higher song complexity does not necessarily correlate with more sensilla, and individual lineages must be carefully analysed for the possibility of such a coevolution between signal and receiver.…”

“…In any case, for ears and dimensions of tympanal membranes and sound guiding structures, there may have been relevant size constraints restricting adaptive changes (e.g. Bailey 1998;Schul and Patterson 2003;ter Hofstede et al 2013;Strauß et al 2014a). Römer et al (2014) recently presented the idea of "acoustic energy catch" in the context of the sensory ecology of pneumorid grasshoppers: any judgment of evolutionary (pre)adaptation should include frequency tuning of the hearing organ, spectrum of the conspecific signal, transmission through the environment and background noise.…”

“…In such duets, both sexes require high auditory sensitivity for mate finding, but for detecting the faint female reply, males are selected to be more sensitive, and, therefore, to have larger acoustic spiracles (e.g. Strauß et al 2014a). However, the female reply has been lost independently in several lineages of the European tettigoniid genus Poecilimon.…”