Evolution of the Metathoracic Tympanal Ear and Its Mesothoracic Homologue in the Macrolepidoptera (Insecta)
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Zoomorphology (1999) 119:93–103 © Springer-Verlag 1999 ORIGINAL ARTICLE Jayne E. Yack · Geoff G.E. Scudder James H. Fullard Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera (Insecta) Accepted: 18 June 1999 Abstract Two independent methods of comparison, se- current phylogenies of the Macrolepidoptera, we demon- rial homology and phylogenetic character mapping, are strate that the three-celled wing-hinge chordotonal or- employed to investigate the evolutionary origin of the gan, believed to be a wing proprioceptor, represents the noctuoid moth (Noctuoidea) ear sensory organ. First, plesiomorphic state from which the tympanal organ in neurobiotin and Janus green B staining techniques are the Noctuoidea evolved. This ‘trend toward simplicity’ used to describe a novel mesothoracic chordotonal organ in the noctuoid ear contrasts an apparent ‘trend toward in the hawkmoth, Manduca sexta, which is shown to be complexity’ in several other insect hearing organs where serially homologous to the noctuoid metathoracic tympa- atympanate homologues have been studied. The advanta- nal organ. This chordotonal organ comprises a proximal ges to having fewer rather than more cells in the moth scolopidial region with three bipolar sensory cells, and a ear, which functions primarily to detect the echolocation long flexible strand (composed of attachment cells) that calls of bats, is discussed. connects peripherally to an unspecialized membrane ventral to the axillary cord of the fore-wing. Homology to the tympanal chordotonal organ in the Noctuoidea is A. Introduction proposed from anatomical comparisons of the meso- and metathoracic nerve branches and their corresponding pe- With the exception of certain degenerate forms (Fullard ripheral attachment sites. Second, the general structure et al. 1997), most members of the Noctuoidea possess (noting sensory cell numbers, gross anatomy, and loca- physiologically sensitive tympanal ears on each side of tion of peripheral attachment sites) of both meso- and the posterior metathorax (Fig. 1). The tympanal mem- metathoracic organs is surveyed in 23 species represent- brane is a thinned region of cuticle that forms part of the ing seven superfamilies of the Lepidoptera. The structure thoracic skeletal framework (Fig. 4b). A chordotonal or- of the wing-hinge chordotonal organ in both thoracic gan, hereafter referred to as the tympanal organ, attaches segments was found to be remarkably conserved in all to the inner surface of the membrane and contains either superfamilies of the Macrolepidoptera examined except one (Notodontidae) or two (all other Noctuoidea) bipolar the Noctuoidea, where fewer than three cells occur in the sensory cells (Eggers 1919). These cells respond best to metathoracic ear (one cell in representatives of the Not- high-frequency sounds (20–50 kHz) and are used to de- odontidae and two cells in those of other families exam- tect the echolocation calls of insectivorous bats and, in ined), and at the mesothoracic wing-hinge (two cells) in some cases, conspecific sounds (see, for example, the Notodontidae only. By mapping cell numbers onto Spangler 1988; Surlykke and Fullard 1989; Sanderford et al. 1998). When a moth hears a bat, a series of evasive flight maneuvers is initiated, which can allow it to es- J.E. Yack (✉) cape predation (for reviews of hearing in the Noctuoidea, Department of Biology, Carleton University see Roeder 1974; Miller 1983; Spangler 1988; Fullard 1125 Colonel By Drive, Ottawa, Ontario, Canada, K1S 5B6 e-mail: [email protected] 1998). Tel.: +1-613-5203887, Fax: +1-613-5204497 All other Lepidoptera lack the external skeletal modi- fications associated with metathoracic ears (Forbes 1916; G.G.E. Scudder Department of Zoology, University of British Columbia Richards 1932). In earlier studies, we described the Vancouver, British Columbia, Canada structure and function of a chordotonal organ located at J.H. Fullard the base of the metathoracic wing in two atympanate Department of Zoology, Erindale College, University of Toronto species, Manduca sexta (Bombycoidea, Sphingidae) and Mississauga, Ontario, Canada Actias luna (Bombycoidea, Saturniidae) (see Yack and 94 Macrolepidoptera, serial homology and phylogeny. We examine a previously undescribed chordotonal organ, and proposed serial homologue of the tympanal organ, in the atympanate mesothorax. We then examine tympanal organs and/or their thoracic homologues in 23 species representing seven ditrysian superfamilies [six from the present study and one from a previous study (Hasenfuss 1997)], and map the evolution of chordotonal organ cell numbers using a recent phylogeny of the Macrolepidop- tera (Kristensen and Skalski 1998). B. Materials and methods I. Taxa examined Table 1 lists the species of Lepidoptera examined in this study. In- dividuals were obtained from four different sources: 1. Actias luna (Linné, 1758), Antheraea polyphemus (Cramer, 1776), Samia cynthia (Drury, 1773), Hyalophora cecropia (Linnaeus, 1758), Manduca sexta (Linné, 1763), and Vanessa cardui (Linné, 1758) pupae were purchased from a commercial supplier (North Carolina Biological, Burlington, N.C., USA). 2. Lirimiris meridionalis Schaus, 1904, one Geometroidea1, and Oxytenis spp. were collected in the field in Panamà. Fig. 1 Lateral view of a noctuid moth, indicating the location of 3. Prionoxystus robiniae (Peck, 1818), Pantographa limata the tympanic cavity (arrowhead) and the abdominal hood (arrow) (Grote and Robinson, 1867), Callosamia promethea (Drury, covering the cavity. The tympanic membrane is situated within 1773), Tolype laricis (Fitch, 1856), T. velleda (Stoll, 1791), the cavity, set within the skeletal framework of the posterior meta- Smerinthis jamaicensis (Drury, 1773), Biston betularia (Linné, thorax 1758), Catocola coccinata Grote, 1872, Pyrrharctia isabella (J.E. Smith, 1797), Lymantria dispar (Linné, 1758), Hetero- campa obliqua Packard 1864, Nadata gibbosa (J.E. Smith, 1797), and Peridea angulosa (J.E. Smith, 1797) were collected Fullard 1990; Yack 1992; Yack and Roots 1992). In both from black-lights at the Queen’s University Biology Station (Leeds County, Ontario, Canada). cases, the atympanate chordotonal organ has three bipo- 4. Trichoplusia ni (Hübner [1803]) were provided by Dr. J. Myers lar sensory neurons, attaches to a non-tympanal mem- from the Department of Zoology, University of British Columbia. brane or cuticle ventral to the axillary cord of the meta- thoracic wing, and appears to function as a proprioceptor detecting vibrations and movements of the hind-wing. It II. Anatomical nomenclature was suggested that the three-celled wing-hinge chordo- Anatomical nomenclature used for muscles and nerves follows tonal organ represents the plesiomorphic, preauditory that of Nüesch (1953, 1957) and Yack and Fullard (1990). Nomen- state and that, through evolutionary modifications of pe- clature relating to tympanal structures was taken from Eggers (1919) and Treat (1959), and terms describing the atympanate me- ripheral structures, the chordotonal organ changed func- so- and metathoracic skeletal structures, from Eaton (1988) and tionally from a proprioceptor to a hearing organ. The hy- Nüesch (1953). pothesis of the proprioceptive origin of lepidopteran tympanal sensilla (von Kennel and Eggers 1933), how- ever, has never been tested systematically. III. Dissection and anatomical procedures Recent studies have demonstrated the value of study- A sagittal dissection approach was used to describe the peripheral ing the evolution of behavioral and morphological traits projections of the mesothoracic IIN1 nerve in M. sexta. Before by mapping these traits onto existing phylogenies of each dissection, the moth was cooled for 30 min. Once cooled, large taxa (see, for example, Brooks and McLennan both the head and abdomen were removed, and the descaled tho- rax was cut in half in a sagittal plane and pinned to Sylgard (Dow 1991; Gwynne 1995), but few have employed phyloge- Corning, Midland, Mich., USA) in a petri dish. Drawings of the netic analyses to learn about the evolution of insect ner- mesothoracic nerve branch IIN1 were carried out by staining and vous systems (see, for example, Shaw and Meinertzha- following the whole branch from the ganglion to the periphery gen 1986; Edgecomb et al. 1995; Strausfeld et al. 1998). with a 0.05% solution of Janus green B in saline (Paul 1974). The branches of IIN1b were traced as closely as possible to their target The evolutionary origin of moth hearing organs can be muscles or tissues and drawn with the aid of a Wild (M3) dissec- conveniently studied using this method, since the ears tion microscope and camera lucida attachment, or photographed. (and their proposed atympanate homologues) consist of Since Janus green B stains only the whole nerve branch lead- very few cells, whose presence or absence can be easily ing to the chordotonal organ (Yack 1993), it was necessary to em- quantified. ploy a second staining method to determine the number of sensory In the present study, we use two comparative methods 1 This individual was identified as a Geometroidea based upon the to examine the evolution of the metathoracic ear in the external skeletal characteristics of the abdominal ear 95 Table 1 Survey of the number of scolopidia (based on number of scolopale caps) in Noctuoidea tympanal chordotonal organs and wing- hinge chordotonal organs of atympanate Lepidoptera. Numbers in parentheses indicate data taken from other studies. (–: Data