Evolution of systems of communication in crickets: a multidisciplinary exploration in space and time

Tony Robillard, Institut Systématique Evolution Biodiversité (ISYEB),

Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE

Adaptive radiations are major drivers of diversification which are triggered by novel ecological opportunities or opening of new niches due to innovations of variable traits, including key features of communication systems. For example, groups of animals that communicate using a particular type of signal that is not used by other species or not detected by predators may diversify more than species using a more occupied signal space, or with more attuned predators.

Most of our understanding of cricket communication derives from studies on field crickets (Gryllinae), in which males emit low frequency calling signals (3-8 kHz) to attract females at long distances, and females find males by phonotaxis. However, crickets in the subfamily Eneopterinae use high frequency signals (>12 kHz) to communicate. This trait has evolved in several clades of this subfamily and may represent a key innovation for an adaptive radiation and the first step in the evolution of a new communication system in the tribe Lebinthini. In this tribe, females lack phonotaxis but reply to the male’s high frequency call by producing vibrations transmitted to the male through the plant substrate (ter Hofstede et al. 2015).

We currently investigate this new system of communication by a broad multidisciplinary approach. In this talk I review some aspects under study by my colleagues and me to understand more precisely the interactions between males and females and the mechanisms involved in extant species. As for any adaptation, clues about past causes can be searched for through the study of the present state, but they can also be investigated by looking back at the spatiotemporal and past ecological context where the change occurred. I present here our progresses to ally biogeographical studies and phylogenetic analyses of cricket communication systems. We combine calibrated molecular phylogenetic studies, biogeographical inferences of ancestral areas and modern phylogenetic comparative methods to investigate the “when” and the “where” of the origin of the new communication system in the tribe Lebinthini. We gathered data about morphology, bioacoustics, habitats and time of activity for a total of 14 traits in 43 species representing all the genera of the subfamily. For each trait, we estimated the ancestral states at each node of the calibrated phylogeny and established the context in which high frequency calls arose based on information about past climates, vegetation and communities of predators and acoustic competitors. With such information, we review the different causes invoked to explain the evolution of high frequency calls and the new system of communication.

Our results suggest that the high frequency calls in the Eneopterinae have evolved multiple times, and that the new system of communication in the Lebinthini originated in South America + Boreotropical region, between late Paleocene and early Eocene (54-60 mya). Strikingly, this date may coincide with the development of high frequency communication in katydids. The diversification of bats also dates back to ca. 60 mya, suggesting that katydids and eneopterine crickets may have convergently evolved high-frequency communication while they faced a rising challenge of bat predation.

Key Words: high frequency, phylogeny, bio-geography, ancestral state reconstruction, adaptive radiation.