Divergent mechanisms of acoustic mate recognition between closely related field cricket species (Teleogryllus spp.)

Abstract

Effective recognition of conspecific mating signals reduces the risk of maladaptive hybridisation. Dissecting the signal recognition algorithms that underlie preferences is a useful approach for testing whether closely related taxa evaluate the same or different signal features to achieve mate recognition. Such data provide information about potential constraints and targets of selection during evolutionary divergence. Using a series of mate choice trials, we tested whether closely-related, but genetically and phenotypically divergent, field cricket species (Teleogryllus oceanicus and Teleogryllus commodus) use shared or distinct recognition algorithms when evaluating acoustic male calling songs. These species overlap in sympatry, show premating isolation based on female discrimination of male calling songs, yet are capable of producing hybrid offspring. Unexpectedly, female selectivity for features of male song differed between the two species. We found that the two species use a combination of shared and unique signal filtering mechanisms, and we characterised how information about male carrier frequency, pulse rate and temporal patterning is integrated to achieve song recognition in each species. These results illustrate how comparatively few, simple modifications in key components of signal recognition algorithms can lead to striking interspecific discrimination among closely related taxa, despite apparent signal complexity. The finding that some steps during signal recognition and filtering are shared between the species, while others differ, can help to identify behavioural traits targeted by selection during evolutionary divergence.

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance

“…Thus, while behavioural isolation may be approximately equal, and strong, in the two species, the behavioural mechanisms by which this isolation is exerted appear to differ. This mirrors findings that female T. commodus and T. oceanicus process and discriminate between species‐specific male calling songs using divergent neurophysiological pattern‐recognition mechanisms (Bailey et al., ).…”

“…However, genomic surveys have not found evidence of gene flow in the field (Moran et al, 2018). Long-range calling song has been suggested to be the primary barrier isolating these species (Bailey, Moran, & Hennig, 2017;Hennig & Weber, 1997;Hill et al, 1972;Hoy & Paul, 1973;Hoy, Pollack, & Moiseff, 1982;Pollack & Hoy, 1979), but female discrimination against heterospecific song does not appear to be sufficiently precise to prevent heterospecific matings. Bailey and Macleod (2014) reported that when females of either species were given a choice between conspecific and heterospecific calling song, up to 25% of the time they chose the heterospecific song.…”

Opposing patterns of intraspecific and interspecific differentiation in sex chromosomes and autosomes

“…Sampling encompassed a c. 2,500 km latitudinal transect along the eastern coastal region of Australia and included allopatric and sympatric populations of both T. commodus and T. oceanicus (Figure ). Areas of sympatry were located with guidance from published studies (Bailey, Moran, & Hennig, ; Hill et al., ; Otte & Alexander, ). Males and females were sampled from each population and preserved in methylated spirits followed by absolute ethanol.…”

“…Species distributions and DNA sampling sites in Australia. T. oceanicus is found across the north (represented by light grey area), while T. commodus (dark grey areas) is mainly restricted to the south‐eastern coast, but has also been documented in the south west (Bailey et al., ; Otte & Alexander, ). Both species overlap in an area ~400 km long on the mid‐eastern coast in Queensland (wavy white lines).…”

A small, computationally flexible network produces the phenotypic diversity of song recognition in crickets

“…The diverse song preferences have been extensively mapped in multiple species (e.g. (Bailey et al, 2017;Cros and Hedwig, 2014;Gray et al, 2016;Hennig, 2003;2009;Hennig et al, 2016;Rothbart and Hennig, 2012a;2012b)) and the song recognition network for one particular species is known . The computation performed by this system -the evaluation of a repetitive pulse pattern -is a common denominator of many communication systems from insects to fish and frogs (Baker et al, 2019;Carlson and Gallant, 2013;Gerhardt and Huber, 2002).…”