The cost of assuming the life history of a host: acoustic startle in the parasitoid fly Ormia ochracea

Abstract

SUMMARYIn the obligatory reproductive dependence of a parasite on its host, the parasite must trade the benefit of 'outsourcing' functions like reproduction for the risk of assuming hazards associated with the host. In the present study, we report behavioral adaptations of a parasitic fly, Ormia ochracea, that resemble those of its cricket hosts. Ormia females home in on the male cricket's songs and deposit larvae, which burrow into the cricket, feed and emerge to pupate. Because male crickets call at night, gravid female Ormia in search of hosts are subject to bat predation, in much the same way as female crickets are when responding to male song. We show that Ormia has evolved the same evasive behavior as have crickets: an acoustic startle response to bat-like ultrasound that manifests clearly only during flight. Furthermore, like crickets, Ormia has a sharp response boundary between the frequencies of song and bat cries, resembling categorical perception first described in the context of human speech. Supplementary material available online at

Evolutionary escalation: the bat–moth arms race

“…These evasive responses are usually graded, meaning that the responses change in a quantitative or qualitative manner with increasing sound amplitude. Almost all other insects with bat-evasive behaviours also show this pattern of graded response, changing from small alterations in flight direction or speed to drastic, last-ditch behaviours as sound amplitude at their ears increases (green lacewings: Miller and Olesen, 1979;crickets: Nolen and Hoy, 1986;mantids: Yager et al, 1990;beetles: Forrest et al, 1995;some katydids: Schulze and Schul, 2001; tachinid flies: Rosen et al, 2009). This is a highly adaptive pattern for bat avoidance.…”

“…Fossil evidence shows that hearing evolved in orthopterans for intraspecific communication before the appearance of bats (Plotnick and Smith, 2012). Tachinid flies that listen for the calling songs of their cricket hosts also had ears before bats evolved (Rosen et al, 2009). For both of these groups, hearing was co-opted for bat detection in addition to still performing its original function.…”

Developing a Phonotaxis Performance Index to Uncover Signal Selectivity in Walking Phonotaxis

“…In principle, our approach could also be applied to quantify signal preferences during flight. Flying phonotaxis has been studied in O. ochracea using a tethered flight paradigm (Rosen et al, 2009). Similarly to crickets, flies adopt steering maneuvers toward stimuli with the temporal pattern and frequency content of cricket calling songs (∼4.5 kHz), but steer away from stimuli with ultrasonic frequencies (>20 kHz) that are characteristic of bat sonar (Wyttenbach et al, 1996;Rosen et al, 2009).…”

“…Flying phonotaxis has been studied in O. ochracea using a tethered flight paradigm (Rosen et al, 2009). Similarly to crickets, flies adopt steering maneuvers toward stimuli with the temporal pattern and frequency content of cricket calling songs (∼4.5 kHz), but steer away from stimuli with ultrasonic frequencies (>20 kHz) that are characteristic of bat sonar (Wyttenbach et al, 1996;Rosen et al, 2009). Developing an index to quantify performance in flying phonotaxis would likely involve measuring response latencies and the magnitude of steering maneuvers to (or away from) the source location.…”

If a bird flies in the forest, does anyone hear it? : avian flight sound cues and hearing in lepidoptera

“…Ormia is also sensitive to sounds in the ultrasonic range and until recently no function had been attributed to this second area of best hearing (Robert et al, 1992). Rosen, et al (2009) found Ormia to elicit an acoustic startle response to ultrasonic stimuli, much like that of their orthopteran hosts. Both the parasitoid fly and its cricket host use hearing for a function other than predator avoidance, yet due to their nocturnal lifestyle and exposure to predators, possess hearing structures that secondarily have evolved to function in predator detection.…”