Behavioral responses of a parasitoid fly to rapidly evolving host signals

Abstract

Animals eavesdrop on signals and cues generated by prey, predators, hosts, parasites, competing species, and conspecifics, and the conspicuousness of sexual signals makes them particularly susceptible. Yet, when sexual signals evolve, most attention is paid to impacts on intended receivers (potential mates) rather than fitness consequences for eavesdroppers. Using the rapidly evolving interaction between the Pacific field cricket, Teleogryllus oceanicus , and the parasitoid fly, Ormia ochracea , we asked how parasitoids initially respond to novel changes in host signals. We recently discovered a novel sexual signal, purring song, in Hawaiian populations of T. oceanicus that appears to have evolved because it protects the cricket from the parasitoid while still allowing males to attract female crickets for mating. In Hawaii, there are no known alternative hosts for the parasitoid, so we would expect flies to be under selection to detect and attend to the new purring song. We used complementary field and laboratory phonotaxis experiments to test fly responses to purring songs that varied in many dimensions, as well as to ancestral song. We found that flies strongly prefer ancestral song over purring songs in both the field and the lab, but we caught more flies to purring songs in the field than reported in previous work, indicating that flies may be exerting some selective pressure on the novel song. When played at realistic amplitudes, we found no preferences–flies responded equally to all purrs that varied in frequency, broadbandedness, and temporal measures. However, our lab experiment did reveal the first evidence of preference for purring song amplitude, as flies were more attracted to purrs played at amplitudes greater than naturally occurring purring songs. As purring becomes more common throughout Hawaii, flies that can use purring song to locate hosts should be favored by selection and increase in frequency.

Assessing patterns of eavesdropper risk on sexual signals and the use of meta-analysis in behavioural ecology: a comment on: ‘The exploitation of sexual signals by predators: a meta-analysis' White et al . (2022)

“…[42]) and re-evolution of novel, safer signals (e.g. [43,44]). White et al acknowledge eavesdropper-induced shifts in signalling behaviour are well documented, but including this evidence in their analysis and interpretations could inform the conclusions more broadly.…”

A novel cricket morph has diverged in song and wing morphology across island populations

“…Here, we document that purring is the most common morph at several sites across Hawaii. Our previous data show that purring attracts females but protects signalling males from the parasitoid fly (Broder et al, 2022;Tinghitella et al, 2021), suggesting that purring males achieve higher fitness than the other morphs in locations where purring has become prominent. This selective advantage could explain the prevalence of purring morphology that we document across Hawaii (Figure 1).…”

“…Purring is a novel sexual signal, and there is quite a lot of variation in the songs produced by different purring males (Tinghitella et al, 2018). We previously demonstrated that population level preferences for existing natural variants of purring songs have not yet developed in female crickets or parasitoid flies (Broder et al, 2022; Tinghitella et al, 2021). While crickets and flies prefer the songs of certain morphs over others (Gallagher et al, 2022; Tinghitella et al, 2018, 2021), the absence of selection on within‐purring variation could allow drift to shape purring differently across populations.…”

“…have not yet developed in female crickets or parasitoid flies (Broder et al, 2022;Tinghitella et al, 2021). While crickets and flies prefer the songs of certain morphs over others (Gallagher et al, 2022;Tinghitella et al, 2018Tinghitella et al, , 2021, the absence of selection on withinpurring variation could allow drift to shape purring differently across populations.…”

“…Since their discovery, purring males have arisen in or spread to several additional locations (Tinghitella et al, 2021) and anecdotally appear to be increasing in prevalence within populations as well. This is likely because of the way natural and sexual selection act on purring; the parasitoid flies greatly prefer ancestral over purring song, and the purr's low amplitude makes it fairly inconspicuous, protecting purring males from parasitism (Broder et al, 2022;Tinghitella et al, 2021). Unlike silent males, however, the purr is attractive to conspecific females (Tinghitella et al, 2018(Tinghitella et al, , 2021, suggesting that purring serves as a private mode of communication among crickets.…”