Novel system of communication in crickets originated at the same time as bat echolocation and includes male-male multimodal communication

Abstract

Understanding the evolutionary origins of communication signals requires careful study of multiple species within a known phylogenetic framework. Most cricket species produce lowfrequency calls for mate attraction, whereas they startle to high-frequency sounds similar to bat echolocation. Male crickets in the tribe Lebinthini produce high-frequency calls, to which females reply with vibrational signals. This novel communication system likely evolved by male sensory exploitation of acoustic startle to high-frequency sounds in females. This behavior was previously described for the Lebinthini from Asia. Here we demonstrate that this novel communication system is found in a Neotropical species, Ponca hebardi, and is therefore likely shared by the whole tribe Lebinthini, dating the origin of this behavior to coincide with the origin of echolocation in bats. Furthermore, we document male duets involving both acoustic and vibratory signals not previously described in crickets, and we tentatively interpret it as competitive masking between males.

Phylogeny, systematics and evolution of calling songs of the Lebinthini crickets (Orthoptera, Grylloidea, Eneopterinae), with description of two new genera

“…Nonetheless, our results offer a framework to study the evolution of acoustic traits in other crickets or orthopteran groups. For example, Tettigonioidea species also produce either low-frequency or ultrasonic calls (Montealegre-Z et al, 2006;Montealegre-Z et al, 2009) and temporal patterns that are either simple or complex (e.g., Heller & Hemp, 2019;ter Hofstede et al, 2020), but phylogenetic studies investigating how spectral features and call complexity evolve in specific groups within this clade are lacking. This can be partly attributed to the enormous effort needed to acquire both taxonomic and biological data for as many species as possible before addressing comparative studies.…”

“…A few clades within the tribe, however, have simpler, monosyllabic calls (i.e., one FW closure produced one call unit), which evolved independently multiple times.Monosyllabic calls could be seen continuous trills with very long silent gaps between syllables, but they function very differently from continuous trills in terms of communication. Several studies in the distantly related species Cardiodactylus muriaRobillard (ter Hofstede et al, 2015) and Ponca hebardiRobillard (Benavides-Lopez et al, 2020) demonstrated that each monosyllabic call provokes one female response and is thus functionally equivalent of the echemes produced by other Lebinthini species. On the contrary, continuous trills likely elicit female phonotaxis.…”

Acoustic signalling in Orthoptera

“…In the bush-cricket Onomarchus uninotatus (Rajaraman et al, 2015) and in lebinthine crickets such as Ponca hebardi (Benavides-Lopez et al, 2020), male and female perform a multimodal duet, where the female responds to the male's calling song by tremulating (making body movements that create vibrations in the substrate). These are true duets, with a clear phase relationship of alternation between the chirps of the male's song and the female's vibrational response.…”

“…Singing and vibrational signals are not always used as alternatives but may instead send different messages. While a P. hebardi male is singing in his duet with the female, he also simultaneously tremulates in response to the songs of other males, sending a vibrational signal similar to that of the female (Benavides- Lopez et al, 2020). The male's vibrations probably serve to mask the female response so that rival males cannot respond to it.…”

Rugabinthus, a new genus of Lebinthina (Orthoptera, Gryllidae, Eneopterinae) from New Guinea

“…Lebinthines have been demonstrated to be important species for the study of insect communication systems. A new communication system using vibrational responses (including vibrotaxis) to high-frequency male calls and population-specific microevolution and plasticity in acoustic properties was recently discovered (ter Hofstede et al 2015, Benavides-Lopez et al 2020, Tan and Robillard 2021a.…”