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.

Keywords: Ormia ochracea; Teleogryllus oceanicus; novelty; parasite–host; phonotaxis; preference.

FIGURE 1

Number of flies captured per trap per night to sound traps broadcasting different song types (ancestral, loud purr, purring, white noise). Sample sizes (traps deployed) are listed above each bar. Bars with the same letter are not significantly different from one another (“loud purr” excluded from Tukey because it caught no flies). Note that there were 128 traps broadcasting purring song (eight exemplars × 16 transects) and 16 of all other stimuli (one each per transect).

FIGURE 2

Behavioral responses to song stimuli (ancestral, loud purr, purring, white noise) in lab‐based phonotaxis tests. Positive responses were measured as (a) distance traveled toward the song stimuli, (b) proportion of flies that contacted the speaker, and (c) average time in seconds to contact the speaker for those that made contact. Bars with the same letter are not significantly different from one another (“white noise” excluded from Tukey in B and C because it caught no flies). Points in A and C represent the raw data, individual fly responses.

FIGURE 3

Preference surfaces describing selection exerted by parasitoid flies across the acoustic space of purring songs (exemplars). Song characteristics of the eight purring exemplars span the PC1 and PC2 axes, and fly responses to those songs are shown on the vertical axis. The gray surface shows the mean response, and the blue and orange layers show the standard error around the mean. Panel (a) shows how far the fly traveled toward the speaker broadcasting the exemplar, (b) shows the proportion of flies that contacted the speaker, and for those flies that contacted the speaker (c) shows the time (s) to contact. Note that for both distance traveled and time to contact, smaller values represent a greater response. See Table 1 for estimates of fixed and random effects.