Evolutionarily conserved coding properties favour the neuronal representation of heterospecific signals of a sympatric katydid species

Abstract

To function as a mechanism in premating isolation, the divergent and species-specific calling songs of acoustic insects must be reliably processed by the afferent auditory pathway of receivers. Here, we analysed the responses of interneurons in a katydid species that uses long-lasting acoustic trills and compared these with previously reported data for homologous interneurons of a sympatric species that uses short chirps as acoustic signals. Some interneurons of the trilling species respond exclusively to the heterospecific chirp due to selective, low-frequency tuning and “novelty detection”. These properties have been considered as evolutionary adaptations in the sensory system of the chirper, which allow it to detect signals effectively during the simultaneous calling of the sympatric sibling species. We propose that these two mechanisms, shared by the interneurons of both species, did not evolve in the chirper to guarantee its ability to detect the chirp under masking conditions. Instead we suggest that chirpers evolved an additional, 2-kHz component in their song and exploited pre-existing neuronal properties for detecting their song under masking noise. The failure of some interneurons to respond to the conspecific song in trillers does not prevent intraspecific communication, as other interneurons respond to the trill.

Neurophysiology goes wild: from exploring sensory coding in sound proof rooms to natural environments

“…Whereas Neuhofer et al ( 2008 ) compared two species with an evolutionary history of long separation, Kostarakos and Römer ( 2015 , 2018 ) investigated the coding of conspecific signals in two closely related sibling katydid species in the Mecopoda elongata complex. They live and communicate in sympatry with rather different signals.…”

“…Thus, a ‘novelty detector’ appears to be present in other katydids as well, and this seems to be adaptive in another behavioural context of predator detection. Kostarakos and Römer ( 2018 ) suggested that chirpers evolved an additional, 2-kHz component in their song and exploited pre-existing neuronal properties that enable them to detect their song under masking noise. In fact, one important element of the sensory drive model (Endler 1992 ; Cummings and Endler 2018 ) is that environmental conditions that are present during signal transmission favour the evolution of signal traits that exploit sensory biases in receivers.…”