The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins

Abstract

A key adaptation for any parasitoid insect is the sensory modality that it uses to locate its host insect. All members of the speciose family Tachinidae (Diptera) are parasitoids, but only flies of the tribe Ormiini use acoustic cues to find their hosts. Ormiine flies are parasitoids of various genera of crickets and katydids. Gravid females of one ormiine species, Ormia ochracea, hear the reproductive calling song of male field crickets and home in on those calls to locate their hosts. While many flies possess various kinds of "ears" to detect airborne sounds, only ormiine flies have been reported to possess true tympanal hearing organs. Such organs are well-known to occur in their cricket and katydid hosts. The ormiine ear is an evolutionary innovation within Diptera. Our objective was to trace the phylogenetic origins of the tympanal hearing organ among higher flies. Since the ormiine hearing organ is a complex organ within the prothorax, we examined possible precursor structures in the prothoraces of selected Diptera. We have uncovered a suite of characters that define the ormiine ear. These characters in the prothorax include a pair of prosternal tympanal membranes, a pair of chordotonal sensory organs, and modifications of the tracheal system. We have been able to identify and trace the presumptive homologs of these ormiine characters through selected species of related Diptera, using the method of outgroup comparison.

Convergent evolution of insect hearing organs from a preadaptive structure

“…In a comparative study, Edgecomb et al (1995) examined the peripheral elements of the sense organ as well as internal elements, like the tracheal system of non-hearing £ies and hearing tachinids to a great detail con¢rming the idea of homologous organs. Anatomically, the organ extends from the sternal apodeme to the presternum (¢gure 1c, f,g, for Sarcophaga bullata).…”

“…Anatomically, the organ extends from the sternal apodeme to the presternum (¢gure 1c, f,g, for Sarcophaga bullata). Also, other prosternal elements of the ears like membranes, sclerotized exoskeletal elements and a large tracheal air sac can be recognized (¢gure 1; Edgecomb et al 1995). The a¡erents project into all three thoracic neuromeres and send collaterals into each respective mVAC (¢gure 2b,e).…”

Structure, development, and evolution of insect auditory systems

“…Two lines of evidence have led to a growing consensus that all known insect tympanal organs derive from chordotonal mechanoreceptors (Boyan, 1993;Edgecomb et al, 1995;Lewis and Fullard, 1996;Meier and Reichert, 1990;Yack and Fullard, 1990;Yack and Roots, 1992;Yager and Scaffidi, 1993). Chordotonal sensilla-sometimes singly, but more of-ten in small clusters-are numerous and widespread throughout the bodies of all insects (Field and Matheson, 1998;McIver, 1985).…”

“…Several comparative studies-both within and among species-show that a group of mechanoreceptors associated with the subgenual organ, also a vibration detector, is clearly the precursor of the ensiferan crista acoustica Lakes-Harlan et al, 1991;Lin et al, 1994). Finally, the precursor of the tachinid fly tympanal organ has been identified in a broad sampling of higher Diptera (Edgecomb et al, 1995;Robert et al, 1996a). The precursor lies in the same location and has a similar structure, but has fewer sensilla (Ͻ40 vs. 70).…”

Auditory Sensitivity of an Acoustic Parasitoid (<i>Emblemasoma</i> sp., Sarcophagidae, Diptera) and the Calling Behavior of Potential Hosts

“…Members of the family Sarcophagidae (Emblemasomatini) use an independently evolved ear [Edgecomb et al, 1995;Robert et al, 1999;Lakes-Harland et al, 1999] to carry out an analogous strategy for finding their hosts, singing cicadas [Soper et al, 1976]. Like that for ormiines, there appears to be interspecific variance in host choice, as several species of flies, found either as larvae or reared to adults, have been collected from various parasitized cicada taxa [Lopes, 1971[Lopes, , 1981Soper et al, 1976].…”