Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history

Abstract

Neoconocephalus Tettigoniidae are a model for the evolution of acoustic signals as male calls have diversified in temporal structure during the radiation of the genus. The call divergence and phylogeny in Neoconocephalus are established, but in tettigoniids in general, accompanying evolutionary changes in hearing organs are not studied. We investigated anatomical changes of the tympanal hearing organs during the evolutionary radiation and divergence of intraspecific acoustic signals. We compared the neuroanatomy of auditory sensilla (crista acustica) from nine Neoconocephalus species for the number of auditory sensilla and the crista acustica length. These parameters were correlated with differences in temporal call features, body size, life histories and different phylogenetic positions. By this, adaptive responses to shifting frequencies of male calls and changes in their temporal patterns can be evaluated against phylogenetic constraints and allometry. All species showed well-developed auditory sensilla, on average 32-35 between species. Crista acustica length and sensillum numbers correlated with body size, but not with phylogenetic position or life history. Statistically significant correlations existed also with specific call patterns: a higher number of auditory sensilla occurred in species with continuous calls or slow pulse rates, and a longer crista acustica occurred in species with double pulses or slow pulse rates. The auditory sensilla show significant differences between species despite their recent radiation, and morphological and ecological similarities. This indicates the responses to natural and sexual selection, including divergence of temporal and spectral signal properties. Phylogenetic constraints are unlikely to limit these changes of the auditory systems.

What determines the number of auditory sensilla in the tympanal hearing organs of Tettigoniidae? Perspectives from comparative neuroanatomy and evolutionary forces

“…However, this correlation so far provides no direct explanation for why a specific number of CA sensilla evolved in a given species. In Neoconocephalus, the number of CA sensilla from nine species was statistically negatively correlated to the species' call frequency (Strauß et al 2017). Since this correlation was also found for the CA length and body size, it was assumed to indicate an allometric relationship (see below), because larger animals have larger stridulatory structures that produce calls in lower frequencies, and body size also influences the number of CA sensilla and CA length.…”

“…By the functions of hearing in mate detection and predator evasion, both sexual and natural selection affect the hearing organs in Tettigoniidae. Adaptations are notable in particular in the size differences of spiracles, which can be related to specific acoustic behaviors and selection pressures between sexes (e.g., Bailey and Römer 1991, Heller et al 1997a, Mason and Bailey 1998, Strauß et al 2017. In some circumstances, evolutionary forces may be difficult to identify by studying only the phenotypes, as selection pressures may overlap or even act in different directions (see Strauß and Stumpner 2015).…”

“…Notably, the number of auditory sensilla is not directly related to the CA length (Schumacher 1979, Lakes and Schikorski 1990, Strauß et al 2017, and between species, fewer sensilla can be found in a longer CA (e.g., . The scolopidial sensilla can occur highly concentrated in the distal CA , Kalmring et al 1995a), leading to pairs or even triplets of somata at the same proximo-distal level (Sickmann et al 1997, Strauß et al 2012.…”

“…The evolutionary diversification is highlighted e.g., by the repeated evolution of double-pulsed calls (Schul et al 2014, Frederick andSchul 2016). Studying the CA anatomy of nine species representing different taxonomic groups, life histories, call patterns, and call center frequencies, similar averages from 32-35 sensilla between the species were documented (Strauß et al 2017). A similar number of 35 sensilla is found in the most closely related Ruspolia (R. nitidula , Schumacher 1979), suggesting that the ancestral Neoconocephalus already had a number of auditory sensilla in these ranges.…”

“…The increased number of sensilla in species with slow-calling rates may be most easy to explain, as they could be an adaptation to shorter signals by providing a relatively stronger input to the CNS by additional sensilla. In addition, indirect effects of acoustic signalling on the CA are likely (Strauß et al 2017). The correlation of discontinuous calls with lower sensillum numbers may depend on the behavioral ecology of signallers since discontinuously calling species have higher population densities (Greenfield 1990), which in turn may relax the selection on the auditory system.…”