m 



of sensory systems, we wanted to know 

 how — and how well — this species of 

 tachinid fly could hear the field crickets. In 

 the course of their lives, both the female 

 cricket and female fly face the same repro- 

 ductive problem: finding a male cricket 

 singing in the dark. The female cricket 

 uses her sense of hearing not only to de- 

 tect and locate singing male crickets but 

 <~] also to recognize those that belong to her 

 Q own species and, possibly, to assess the 

 ,_, adequacy of the male by the quality of his 

 *—> song. For the fly, the task is also to find a 

 [ZS cricket of the right species. The possibihty 

 -H that a female fly also assesses the quality 

 O or health of her host before entrusting her 

 J> brood to him seems sUm, but cannot be 

 ruled out. 



Our probing of its anatomy reveals that 

 the hearing organ of 0. ochracea is com- 

 posed of a pair of very thin membranes sit- 

 uated on the front of the thorax, near the 

 neck and just behind the head. These 

 membranes act much as human eardrums 

 do, converting sound energy into mechan- 

 ical movements. Each membrane is 

 backed by an air chamber and attached in- 

 ternally to a vibration sensor. The ear ap- 

 pears to have evolved from a chordotonal 

 sensory organ, a type of "mechanorecep- 

 tor." In nonhearing flies this organ serves 

 as a sort of strain gauge that senses 

 stresses around the neck region and prob- 

 ably helps monitor the movement and pos- 

 ture of the head and front legs. 



Although an exceptional anatomical de- 

 velopment among flies, the tiny ears re- 

 semble those found in various other in- 

 sects, including crickets. In all cases that 

 have been studied, insect ears seem to 

 have evolved from such chordotonal or- 

 gans. In crickets, for example, ears 

 evolved from sensors situated on the tibia 

 of the fi-ont legs, which originally func- 

 tioned merely to detect low-frequency 

 ground vibrations. Various lines of evi- 

 dence suggest that the original sensory 

 structure was duplicated, and that this du- 

 plicate gained a separate function, the 

 sensing of air vibrations. As in other in- 

 sects with ears, these structures have noth- 

 ing in common with the feathery antennae 

 that enable some insects (mosquitoes, for 

 example) to detect low-pitched sounds, 

 such as the buzzing of other insects, at 

 close range. 



The fly's ear resembles the cricket's not 

 only in structure and sensory origin but 

 also in sensitivity. One way to understand 

 a fly's sensitivity to sound is to measure 

 the electrical activity of the sensory nerves 

 leading from its ears to its central nervous 



system. To determine which pitches 0. 

 ochracea is most sensitive to, we inserted 

 tiny recording electrodes into the thorax, 

 at the base of the auditory nerves, and 

 tested the reaction to computer-generated 

 simulations of the cricket's song. 



Our experiments have demonstrated 

 that this tiny fly is most sensitive to sounds 

 at the frequency of five kilohertz (a little 

 above the highest pitch on the piano), a 

 pitch close to the frequency that dominates 

 the cricket's song. This is a striking ex- 

 ample of a phenomenon known as conver- 

 gent evolution, where superficially similar 

 structures evolve in distanfly related or- 

 ganisms as adaptations to similar require- 

 ments or circumstances. 



The fly's sensitivity — and especially 

 that of the female fly — even surpasses the 

 cricket's. We estimate that a female cricket 

 can detect a male cricket from at least 

 twenty yards away, while the fly can hear 

 it from twice that distance. (Humans we 

 tested are even more sensitive, discerning 

 the cricket song at sixty yards — but they 

 are not as quick and precise at locating it in 

 the grassy meadows, perhaps for lack of 

 practice.) 



In field experiments using loudspeak- 

 ers, we have shown that the flies are at- 

 tracted by the sound of the cricket and re- 

 quire no other cues, such as smell. If the 

 flies' ears are damaged, they cannot locate 

 the sound. On the other hand, prehminary 

 observation suggests that they may be re- 

 luctant to deposit their larvae unless they 

 actually find a cricket at the source of the 

 sound. In contrast, entomologist Tom 

 Walker and his colleagues at the Univer- 

 sity of Florida, Gainesville, have observed 

 that a related species from Brazil, O. de- 

 pleta, will readily deposit from one to 

 eight maggots right on a piece of paper 

 covering a loudspeaker. 



So far, six members of the genus Ormia 

 are known to have ears for detecting their 

 insect hosts, an ability they must have in- 

 herited from their common ancestor. In ad- 

 dition to field crickets, their specific hosts 

 include some katydids and mole crickets. 

 Two genera of flesh flies have also 

 evolved, independently, a remarkably sim- 

 ilar hearing organ to hsten for the singing 

 of cicadas. 



To be a successful bacterium, fungus, 

 animal, or plant depends on detecting cru- 

 cial features of the environment. Survival 

 often requires diverse sensory capacities. 

 From an evolutionary perspective, there is 

 always a potential advantage in doing 

 something a little differently. When some 

 parasitoid flies gained ears, a whole new 



Guided by her acute sense of 

 hearing, a female fly has located a 

 cricket host for her brood. 



Daniel Robert; Cornell University 



sensory world became accessible to them. 

 They reaped the advantage of locating a 

 dispersed, concealed host. Other flies 

 could find crickets by sight or smell, but 

 might miss some that are easily located by 

 sound. The hearing flies filled a new niche, 

 where competition was reduced and re- 

 sources lay untapped. 



Despite the advantage hearing has con- 

 ferred on certain species of parasitoid flies, 

 the phenomenon is not widespread. Shel- 

 ley Adamo, of Cornell University, who 

 studies the effects of parasitism on cricket 

 behavior, physiology, and reproductive 

 success, has concluded that at least in 

 North America, relatively few singing in- 

 sect species have bodies large enough to 

 support a tachinid infestation. Probably 

 more remain to be discovered in the trop- 

 ics, where singing insects are numerous — 

 and often large. 



Many questions remain to be explored 

 in the relationship between ear-equipped 

 tachinid flies and their hosts. What effect 

 do the parasitoids have on the cricket pop- 

 ulation as a whole? How detrimental is in- 

 festation to a male cricket's ability to leave 

 offspring? And will the cricket's tendency 

 to chirp eventually be eliminated by nat- 

 ural selection? 



Some cricket species have lost their 

 ability to sing, and we and others suspect 

 that parasitism played a key role in this 

 loss. Males of the species Gryllus ovi- 

 sopis, whose common name is the taciturn 

 field cricket, lack a long-range call, al- 

 though they conserve enough of the 

 sound-producing wing anatomy to scrape 

 out a short-range courtship song if a fe- 

 male wanders into range. According to 

 Tom Walker, who has studied them, they 

 do not seem to have evolved any other 

 long-range signals, such as chemicals. An 

 entirely mute species (which has also lost 

 its ears) is Larandeicus bicolor of south- 

 em Africa. Unlike its singing relatives, it 

 attracts a female's attention with its 

 brightly colored wings. Crickets may 

 never regain the freedom of action they 

 lost when tachinid flies arose forty million 

 years ago. But if the going gets too tough, 

 they may evolve some new tricks of their 

 own. 



50 Natural History 6/94 



