Download Structure, development, and evolution of insect auditory systems

MICROSCOPY RESEARCH AND TECHNIQUE 47:380–400 (1999)
Structure, Development, and Evolution
of Insect Auditory Systems
DAVID D. YAGER*
Department of Psychology, University of Maryland, College Park, Maryland 20742
KEY WORDS
ears; scolopale; sound reception; chordotonal organ; tympanum; directional
hearing
ABSTRACT
This paper provides an overview of insect peripheral auditory systems focusing on
tympanate ears (pressure detectors) and emphasizing research during the last 15 years. The theme
throughout is the evolution of hearing in insects. Ears have appeared independently no fewer than
19 times in the class Insecta and are located on various thoracic and abdominal body segments, on
legs, on wings, and on mouth parts. All have fundamentally similar structures—a tympanum backed by a
tracheal sac and a tympanal chordotonal organ—though they vary widely in size, ancillary structures, and
number of chordotonal sensilla. Novel ears have recently been discovered in praying mantids, two families
of beetles, and two families of flies. The tachinid flies are especially notable because they use a previously
unknown mechanism for sound localization. Developmental and comparative studies have identified the
evolutionary precursors of the tympanal chordotonal organs in several insects; they are uniformly
chordotonal proprioceptors. Tympanate species fall into clusters determined by which of the embryologically defined chordotonal organ groups in each body segment served as precursor for the tympanal
organ. This suggests that the many appearances of hearing could arise from changes in a small
number of developmental modules. The nature of those developmental changes that lead to a
functional insect ear is not yet known. Microsc. Res. Tech. 47:380–400, 1999. r 1999 Wiley-Liss, Inc.
INTRODUCTION
Hearing plays a crucial role in the lives of many insects:
for some it provides a means to detect and evade predators,
others use species specific acoustic signals to locate and
select appropriate mates, and a few parasitoids home in on
singing insects as hosts for their hungry offspring (Bailey,
1991). Although only a small proportion of all insect species
can hear, the diversity of insect ears is astonishing: we
know of at least 19 independent evolutions of audition
among insects and that number is certain to grow. There is
hardly a body part that does not, on some insect, sport an
ear, and that includes wings, legs, and mouth parts.
The goal of this paper is to provide overview of insect
peripheral auditory systems. It will be selective in two
senses: (1) there will be a strong emphasis on discoveries and developments in the last 15 years. Details of
earlier work are readily available in the excellent and
comprehensive review by Michelsen and Larsen (1985).
The mid-1980s also marked the beginning of a renaissance in the field of insect audition with the discovery of
several ‘‘new’’ ears and, even more importantly, a shift in
emphasis toward attempts to understand the evolution of
insect auditory systems using developmental and comparative strategies; (2) this paper will deal only with pressure
detection. The important topic of near-field sound reception
(usually low frequency sound detected by socketed hairs) is
well reviewed by Römer and Tautz (1992).
FUNDAMENTALS OF THE PRESSURE
RECEIVER
Detection of the pressure component of sound allows
sensitive detection of acoustic signals over long distances, whereas velocity and acceleration detection are
r 1999 WILEY-LISS, INC.
limited to short distances and low frequencies (Römer
and Tautz, 1992). Since the efficiency of signal production for small creatures like insects increases dramatically for frequencies greater than a few kilohertz (Michelsen, 1992), pressure-detection hearing makes
particularly good sense for intraspecific communication. All animals, vertebrate and invertebrate, use a
sensory organ of the same basic structure—the tympanate ear–for this purpose.
Functional Anatomy
The tympanate ear comprises three anatomical and
functional parts: the tympanum, the tracheal sac, and
the tympanal organ (shown in Fig. 1 using the noctuid
moth ear as an example).
The tympanum is simply a region of very thin cuticle
that is set into vibration by the oscillating difference in
pressure between its two sides (Figs. 1, 3, 5). The
typical insect tympanum is round or oval and membranous in appearance. Tympanal thickness in insects
ranges from 1 µm in cicadas (Young and Hill, 1977) to
40–100 µm in wetas (the ensiferan family Stenopelmetidae; Ball and Field, 1981). There is often a distinct
cuticular rim around its circumference that may help
isolate it from body movements. Green lacewings (Neuroptera) have the smallest of known insect tympana
with an area of 0.02 mm2 (0.6 mm longest dimension;
Miller, 1970); the area in cicadas (Homoptera) may
Contract grant sponsor: University of Maryland, College Park.
*Correspondence to: David D. Yager, University of Maryland, College Park, MD
20742. E-mail: [email protected]
Received February 1999; accepted in revised form June 1999
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381
Fig. 1. A: The ears of noctuid moths like this Catocla sp. are on the
dorsolateral thorax at the junction with the abdomen (arrow). B:
Horizontal section through the right ear of a noctuid. The tympanum
(ty) is thinned cuticle backed by tracheal sacs (ts). The tympanal
organ (to) with its two scolopidia attaches to the center of the
tympanum and is supported by a ligament (lg). The tympanal nerve
(tyn) has the axons of the auditory afferents (A1 and A2) and the axon
of the non-auditory B cell associated with the Bügel (bg). Photograph
reproduced from Brackenbury J. 1992. Insects in flight. London:
Blandford. 192 p., with permission.; drawing modified from Roeder
KD, Treat AE. 1957. Ultrasonic reception by the tympanic organ of
noctuid moths. J Exp Zool 134:127–157.
reach 4 mm2 (Young and Hill, 1977). The circular,
uniform noctuid moth tympanum described below is
one of the simplest among insects (Fig. 1). More complex tympana are non-homogeneous in thickness and
sometimes have cuticular structures on the tympanum
itself that affect vibration (some aquatic hemipterans,
for instance, have a club-like appendage; Prager, 1976).
The tympanum of locusts is among the most complex. It
is divided into four regions, each associated with a
group of sensilla in the tympanal organ (Müller’s
organ). A complex interaction between the frequencydependent tympanal vibration in each region and the
separate biomechanical characteristics of Müller’s organ yields frequency discrimination based on a ‘‘place
code’’ functionally analogous to that of the mammalian
cochlea (Breckow and Sippel, 1985; Inglis and Oldfield,
1988; Stephen and Bennet-Clark, 1982).
The pressure changes of a sound wave will have little
effect on a membrane unless the medium on the inner
side of the membrane has a characteristic acoustic
impedance (a function of density) matched to that of the
external medium. For this reason, animals listening to
airborne sound have an air space or air sac on the
internal side of the tympanum; the mammalian middle
ear is an example. For insects, this is an enlarged
trachea or a tracheal sac tightly apposed to the inner
surface of the tympanum (Figs. 1, 3, 5). There are rare
exceptions: the green lacewing (on the radial vein of the
wing; Miller, 1970) and some—but not all—aquatic
hemipterans (on the mesothorax and metathorax; Arntz,
1975) have tympana backed by fluid.
The tympanum converts the pressure changes of a
sound wave to an in-and-out motion of the membrane.
This mechanical signal must be transduced to neural
signals—the function of the tympanal organ. This is
made up of chordotonal sensilla (also called scolopidia;
Fig. 2) that do not appear to be substantially modified
for sound reception as opposed to their mechanoreceptive functions throughout the insect body; they are
classified as Type 1 sensilla (McIver, 1985). Field and
Matheson (1998) provide extensive and excellent review of chordotonal organ anatomy and function. In
tympanal chordotonal sensilla, a modified stereocilium
with a 9*2⫹0 structure that originates in the dendrite
of the single bipolar sensory neuron extends through a
tubular space formed by the scolopale cell and inserts
into the extracellular scolopale cap (Fig. 2B). The
scolopale rods are intracellular structures composed of
densely packed microtubules that form a sleeve around
the cilium and also attach to the cap. An attachment
cell surrounds the distal portion of the scolopale cell
and the scolopale cap; it links the scolopidium to the
vibrating membrane directly or through a ligament (for
instance, Fig. 5C, D). In this way, the sensillum can be
stretched by the differential movement between the
tympanum and the less movable cell body with its
surrounding glial cells. In a few cases (geometrid
moths, cicadas, mantids; Kennel and Eggers, 1933;
Michel, 1975; Yager and Hoy, 1987), some or all of the
scolopidia in the tympanal organ have an inverse
anatomy with the scolopales pointed away from the
tympanum—the attachment cell anchors the sensillum
to a relatively motionless structure and the opposite
end is connected directly or indirectly to the tympanum.
In terms of stretching the sensillum, this is mechanically equivalent to the more normal case, and the
significance of these inversions is not known. The
chordotonal sensilla of all tympanal organs studied to
date are mononematic (the dendritic cilium attaches
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D.D. YAGER
Fig. 2. A: Schematic drawing of three chordotonal sensilla in a
tympanal organ. The somata of the bipolar sensory neurons (b) are
surrounded by accessory cells (ac). The scolopale cell (sc) surrounds
the dendrite of each neuron. Attachment cells (at) link the scolopidia
with the tympanum (ty). B: Enlargement of the boxed region in A
showing the relationship between the cilium of the neuron, the
scolopale rods, and the scolopale cap. The locations of the two
transverse sections are indicated by the dashed lines. Note that the
cilium and the rods are all attached to the extracellular cap, and the
cap is embedded in the attachment cell. Modified from Gray EG. 1960.
The fine structure of the insect ear. Phil Trans R Soc B 243:75–94..
directly to a scolopale cap rather than a tube) and
monodynal (one bipolar neuron per sensillum).
Tympanate insects vary widely in the number of
scolopidia in the tympanal organ. There is only one
chordotonal sensillum in the tympanal organ of notodontid moths (Surlykke, 1984) and sphinx moths (Göpfert
and Wasserthal, 1999b). There are 1,300–1,500 in
cicadas (Michel, 1975; Young and Hill, 1977) and almost
2,000 in the primitive pneumorid grasshoppers (van
Staaden and Römer, 1998). Many insect tympanal
organs have 50–100 scolopidia. There is as yet no
satisfactory explanation for this diversity. The number
of sensilla does not correlate well with absolute sensitivity. In a case such as the pneumorids (described in more
detail below) where distance from the calling male
affects the behavior of the female, the large number of
scolopidia could provide intensity range fractionation
for improved relative intensity measurement. Physiological evidence of intensity range fractionation comes
from noctuid moths (see below) and some tettigoniids
where several receptor cells tuned to the same frequency have substantially different thresholds (Kalmring et al., 1978). The analogous range fractionation for
sound frequency occurs in the tympanal organs of
ensiferans where there is a linear, tonotopic arrangement of sensilla (Oldfield, 1982; Oldfield et al., 1986;
Stumpner, 1996), but Kalmring et al. (1990) did not find
increased frequency range or resolution with increasing sensillum number among seven species of tettigoniid.
The necessary and sufficient stimulus for generating
a receptor potential in the bipolar neuron of an auditory
scolopidium is a longitudinal stretch of the cilium.
While it seems evident that deformation of the cilium
must lead to permeability changes that, in turn, generate a receptor potential (French, 1988), little is known
about the actual mechanism. In other systems, it is
clear that tension does not simply ‘‘stretch open’’ holes
in the membrane to increase permeability; the response
is due to the opening of specialized channels (French,
1992). These mechanically activated channels have
been found throughout the animal kingdom, and their
opening most often non-specifically increases the flow of
monovalent cations (Hoger et al., 1997). However, they
have not yet been unequivocally demonstrated in insect
Type I sensilla.
The axons of the bipolar neurons terminate in the
CNS in an auditory neuropile where they synapse with
local and intersegmental auditory interneurons (reviewed in Michelsen and Larsen, 1985; Pollack, 1998).
The afferent projections of all species studied to date
are solely ipsilateral. In some insects, the auditory
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neuropile is entirely within the ganglion of the same
body segment as the ear (crickets, tettigoniids), but
more commonly, the afferents send branches into one or
more adjacent ganglia (locust, cicada, mantis, tachinid
fly). Where it has been identified, the region of the
ganglion occupied by the auditory afferents is quite
consistent across taxa (Ball and Field, 1981; Boyan et
al., 1990; Esch et al., 1980; Halex et al., 1988; Römer et
al., 1988; Wohlers et al., 1979; Yager and Hoy, 1987).
The dominant and most consistent area is a dense
neuropile just ventral to the ventral intermediate tract
(VIT) known as the medial ventral association center
(mVAC; also called the anterior intermediate sensory
neuropile and the anterior ring tract, but these terms
are not consistent with established CNS naming conventions; Field and Matheson, 1998; Pflüger et al., 1988).
This is an established mechanoreceptive processing
region that receives chordotonal input in other insects
(Hustert, 1978; Merritt and Whitington, 1995; Pflüger
et al., 1988). Auditory terminations in mantids are
unconventional (Yager and Hoy, 1987). In orthopterans,
the afferents are grouped by their optimal frequency
range; this division persists in mVAC in the form of a
tonotopic organization (Halex et al., 1988; Römer, 1983;
Römer et al., 1988; Stumpner, 1996; Wohlers and
Huber, 1985).
Capabilities
Tympanate ears offer the advantages of good sensitivity at high frequencies and effective operation over a
broad frequency range. Auditory thresholds for the
most sensitive insects—pneumorid grasshoppers, for
instance (van Staaden and Römer, 1998)—are in the
range of 0–20 dB re: 20 µPa (⫽dB SPL), comparable to
most mammals. For the majority of tympanate insects,
best sensitivity is between 30 and 50 dB SPL, and there
are some (nymphalid butterflies, some mantids) that
are less sensitive (60–70 dB SPL). It is worth noting,
however, that threshold comparisons across studies are
difficult to interpret because of differences in measurement technique and threshold criteria. Michelsen and
Larsen (1985) provide a less ambiguous summary from
the literature: a vibrational displacement amplitude of
1 Å is sufficient to stimulate tympanal receptors of
crickets, tettigoniids, locusts, and noctuid moths. Sphingid moths are also at least this sensitive (Roeder, 1972).
For small animals like insects, the physics dictates
that tympanate hearing below 1–2 kHz is rarely feasible (Michelsen, 1992), but many insect ears (crickets
and cicadas, for instance) are tuned to match speciesspecific calling songs in the 2–6 kHz range. A number of
insects—additionally or exclusively—have ultrasonic
hearing for bat detection or for intraspecific communication or for both. Maximal sensitivity is most commonly
at 30–60 kHz, the same frequency range most used by
bats for their echolocation cries. Some pyralid moths
(Spangler, 1987), tettigoniids (Morris et al., 1994), and
mantids (Triblehorn and Yager, 2000) have their best
hearing at frequencies ⱖ100 kHz. Not surprisingly,
auditory system tuning for intraspecific communication
tends to be much narrower than for predator evasion.
Virtually all hearing animals have two ears widely
separated on the body, and this serves a vital behavioral function. By comparing the intensity or phase or
time of arrival of sound at the two ears, an animal can
determine the direction to a sound source; Michelsen
(1998) provides a detailed review for insects. The
pattern of two widely-separated ears holds for almost
all insect auditory systems, but there are exceptions:
praying mantids have a single ear in the ventral
midline and lack directional hearing (Yager and Hoy,
1989); the auditory organs on the mouth parts of
sphingid moths are near the midline and non-directional (Göpfert and Wasserthal, 1999a; Roeder, 1972);
tachinid flies have two ears very close together on the
anteroventral thorax, but achieve directionality through
a novel bioacoustic mechanism (Miles et al., 1995; Fig.
7). Ears on wings (green lacewings and two lepidopteran groups) pose a special problem since the ears are
in constant motion during flight when hearing is behaviorally important. Green lacewings do not show evidence of auditory directionality (Miller, 1984).
BRIEF OVERVIEW OF INSECT EARS
Taxonomic Distribution
Tympanate hearing is scattered throughout the insect world with no obvious taxonomic pattern. Figure 3
shows the known distribution among orders and gives
the minimum number of independent evolutions within
each order. The pattern is patchy even at lower taxonomic levels in some otherwise tympanate lineages
because of secondary loss (Gwynne, 1995; Otte, 1990;
Yager, 1990).
Locations on the Body
At first impression, about the only place that insects
seem not to have ears is on the sides of their head. Legs,
mesothorax, metathorax, abdomen (various segments),
wings, mouth parts are all home for ears in some group
(Yack and Fullard, 1993). By far the most commonly
eared body region is the caudal thorax/rostral abdomen
(T2 – A2); this is the location of 12 of the 19 known
peripheral auditory systems. There are several possible
reasons for this: it is often the widest part of the body
and hence provides greatest directional cues; the delicate tympana may be less vulnerable to damage; there
are more and larger trachea and tracheal sacs available
for impedance matching.
Two Contrasting Examples
Noctuid Moths. Anatomically, the noctuid ear is
one of the simplest among insects. It is typical of moths
in the superfamily Noctuoidea, which includes the
noctuids, arctiids, notodontids, and allied families. The
anatomy has been described by Eggers (1919), Richards
(1933), Roeder and Treat (1957), and Ghiradella (1971)
and reviewed by Spangler (1988a).
The two ears are positioned on the dorsolateral
thorax at the junction with the abdomen (Fig. 1A). Each
tympanum lies in a shallow cavity that in most cases
has a movable covering or ‘‘hood.’’ They face posteriorly
(more ventrally in arctiids). The shape is approximately
circular with a diameter in the range of 0.5–2 mm
depending on the size of the moth. There is a rim of
dense cuticle; a short projection (the ‘‘Bügel’’) from the
medial rim extends into the body (Fig. 1B). The tympanal membrane is typically 0.5–1.0 µm thick and quite
delicate. Behind the tympanum is a large tracheal sac
that increases sensitivity (by impedance matching), but
384
D.D. YAGER
Fig. 3. A recent phylogeny of the neopteran insects showing the
orders in which at least some species have tympanate auditory
systems. The numbers indicate the currently recognized number of
independent evolutions of hearing in each order. Audition is not know
in the apterygote insects (bristletails, silverfish) nor in the Palaeoptera (dragonflies, mayflies). Dashed lines indicate less certain relationships. Modified from Kristensen NP. 1991. Phylogeny of extant
hexapods. In: CSIRO. The insects of Australia. Ithaca, NY: Cornell
University Press. p 125–140..
apparently does not play any significant role in tuning
or directionality.
The tympanal organ comprises two chordotonal sensilla of typical structure (but only one in notodontids;
Surlykke, 1984) fixed by attachment cells directly to the
center of the tympanum (Fig. 1B; Ghiradella, 1971;
Yack and Roots, 1992). The two afferent neurons, the A1
and A2 cells, have the same broad tuning to 25–50 kHz,
but the A1 cell has a lower threshold by approximately
20 dB (Roeder, 1967). The lowest thresholds for noctuid
moths are generally 30–50 dB SPL, although a few
species are more sensitive. A third sensory neuron, the
B cell, attaches to the Bügel; it is a proprioceptor that
does not respond to sound.
The tympanal nerve with its three axons travels to
the metathoracic ganglion. A1 sends branches caudally
to the first abdominal segment and rostrally to the
mesothorax with a few fibers extending to the brain; A2
stays almost exclusively in the metathoracic ganglion
(Paul, 1973; Surlykke and Miller, 1982). The presynap-
tic terminals of both afferents lie primarily in mVAC,
but some branches of A2 terminate more dorsally
(Boyan et al., 1990). There are at least ten bilateral
pairs of interneurons originating in the metathorax and
mesothorax that receive strong auditory input, and
most send their axons to the brain (Boyan and Fullard,
1986, 1988; Boyan and Miller, 1991; Boyan et al., 1990).
Despite the relative simplicity of the auditory system, noctuids are capable of performing evasive maneuvers in response to bat echolocation cries that are
appropriate in direction and behavioral intensity to the
location of the approaching bat (reviewed in: Fullard,
1998; Roeder, 1967). The intensity range fractionation
provided by the A1 and A2 cells underlies a switch in
type of escape behavior as the distance between bat and
moth decreases. The maneuvers increase the probability of survival by 40–50%. Some species of noctuoid
moths have additionally (and secondarily) incorporated
acoustic signaling into their courtship (for instance:
Conner, 1987; Sanderford and Conner, 1990).
Crickets and Bushcrickets. The ears of the orthopteran suborder Ensifera (crickets, bushcrickets, weta,
and allied families) differ in several anatomically and
functionally important ways from the simple ears of
moths (Bailey, 1990; Ball and Field, 1981; Ball et al.,
1989; Mason, 1991; Michel, 1974). Most obvious is
location: ensiferan ears are on the proximal tibiae of the
prothoracic legs (Fig. 4A). Crickets and bushcrickets
have two tympana on each tibia. In the former, they are
exposed on the anterior and posterior surface; the
anterior tympanum plays little, if any, role in sound
reception. Bushcrickets also have an anterior and posterior tympanum on the tibia (both of which contribute to
sound reception), but they are most often in slits or
chambers. The diversity of these structures associated
with the tympana in tettigoniids is remarkable, and
their effects on hearing have been a source of extended
debate. Some data (reviewed in Bailey, 1990) suggest
that they confer heightened sound localization favoring
the direction of the slit openings, and that, at least in
some cases, the slits/cavities may play an important
role in tuning the auditory response. However, other
authors (Lewis, 1974; reviewed in Michelsen, 1992;
1998) have pointed out that even for larger bushcrickets calling at high frequencies, the sound wavelengths
are long compared to the dimensions of the slits and
chambers. In this situation, the bioacoustics predict a
negligible effect of the accessory structures on tympanal vibration, and measurements have shown minimal
diffraction of sound by the leg (Michelsen et al., 1994a).
The posterior tympanum of a medium-size cricket
like Teleogryllus commodus is oval, with dimensions of
approximately 0.8 ⫻ 0.3 mm; the tympanal thickness is
2–4 µm (Young and Ball, 1974). The vibration characteristics of the tympanum—especially the role played by
the tympanum in tuning the auditory system—have
been controversial. Recent studies on crickets (Larsen
et al., 1989; Popov et al., 1994) and bushcrickets
(Bangert et al., 1998) have found that the tympanum is
not strongly tuned to the calling song, which suggests a
secondary source of tuning in the mechanics of the
vibration of trachea or associated tissue or in the
mechanics of the receptor cells themselves.
A large tracheal expansion is apposed to the inner
surface of the tympanum (Fig. 4B,C). The tympanal
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385
Fig. 4. A: The oval tympana of crickets are on the prothoracic legs
just below the femurotibial joint. In this Australian species (Homoeoxipha lycoides), the anterior tympana (visible here) are as large as the
posterior tympana; in most crickets the anterior are smaller than the
posterior. B: A cut-away view of the proximal tibia of Gryllus bimaculatus. The tympanum is beneath the enlarged trachea (ts) and not
visible. Thy tympanal organ (to) is a linear array of scolopidia situated
on the trachea; the scolopale caps are directed toward the attachment
to the cuticle. C: A transverse section through the tibia at the level
indicated by the dotted line. The thin posterior tympanum (pty) is the
primary source of acoustic input; the anterior tympanum (aty) is thick
and without tracheal backing. A reproduced from Otte D, Alexander
RD. 1983. The Australian crickets. Monograph 22. Philadelphia:
Academy of Natural Sciences. 477 p, with permission of the publisher.
B and C modified from Michel K. 1974. Das Tympanalorgan von
Gryllus bimaculatus DeGeer (Saltatoria, Gryllidae). Z Morph Tiere
77:285–315..
tracheal sac is part of a tracheal system that is open to
the exterior through the enlarged first thoracic spiracle
and that communicates with the spiracle and tympanal
air sac on the contralateral side. In contrast to moths,
the tracheal system plays a crucial role in sound
reception beyond simple impedance matching by providing access for sound to the inner surface of the tympanum. The force moving the tympanum is the net
pressure resulting from sound striking the inner and
outer surface, which, in turn, is a complex function of
sound frequency along with the geometry and acoustics
of the tracheal system (a ‘‘pressure difference’’ receiver;
Michelsen, 1998). In crickets, tympanal motion is determined by both the sound striking the external surface
and the sound reaching the internal surface through
the ipsilateral and contralateral spiracles (Michelsen et
al., 1994b). The internal routes introduce phase delays
that vary with direction; at the calling song frequency
the contribution from the ipsilateral spiracle is about
three times larger than that from the contralateral
spiracle, but the latter is crucial for directional hearing.
The situation in bushcrickets is quite different. The
spiracle and trachea are highly specialized and show
considerable variation across taxa. The ipsilateral tra-
chea acts as a sound guide with significant gain leading
to the back of the tympanum, and in many cases is the
dominant source of input to the ear. It also may play a
significant role in the tuning of the auditory system.
When the internal sound route dominates, the tettigoniid ear functions as a pressure rather than a pressure
difference receiver, and directional cues come from
diffraction (‘‘sound shadowing’’) around the thorax
(Michelsen et al., 1994a).
The tympanal organ in these insects (the ‘‘crista
acoustica’’) is not attached directly to the tympanum,
but to the wall of the tympanal tracheal sac (Fig. 4B,C).
It is a linear array of 60–70 chordotonal sensilla (20–50
in bushcrickets) oriented along the longitudinal axis of
the tibia. Intracellular recordings from individual bipolar sensory neurons at different locations along the
array have demonstrated a tonotopic organization:
distal sensilla respond to higher frequencies and proximal sensilla to lower frequencies (Oldfield, 1982; Oldfield et al., 1986; Stumpner, 1996). The number of
sensilla devoted to each portion of the overall frequency
range varies with species (Kalmring et al., 1990; Oldfield, 1984, 1988). Typically, the receptors cluster in
three frequency ranges: the greatest number are tuned
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D.D. YAGER
around the calling song frequency (3–5 kHz for most
crickets), and the smallest number have best frequencies over 19 kHz (Imaizumi and Pollack, 1999).
The auditory afferents travel to the prothoracic ganglion in the leg nerve (Nerve 5); they form a dense
auditory neuropile in mVAC. The tonotopy that originates with the receptors is preserved in the organization of the auditory neuropile (Oldfield, 1983; Römer,
1983; Römer et al., 1988; Stumpner, 1996). There are at
least seven bilateral pairs of auditory interneurons,
and their physiology and role in processing auditory
information have been studied extensively (reviewed
in: Pollack, 1998; Schildberger et al., 1989).
The fossil record (Carpenter, 1992) and comparative
studies (Gwynne, 1995) suggest that the earliest—and
still dominant—function of hearing in the Ensifera was
intraspecific communication. After the appearance of
echolocating bats 65–85 million years ago (Novacek,
1985), many lineages added bat evasion based on
ultrasonic hearing (Libersat and Hoy, 1991; Mason et
al., 1998; Nolen and Hoy, 1986), although there are
many instances of secondary loss of this function accompanying brachyptery and flightlessness (Otte, 1990).
RECENT DEVELOPMENTS
Newly Discovered Ears
Dictyoptera
Praying mantids (suborder Mantodea). Praying mantids are highly visual, diurnal predators, and their huge
eyes largely defined our perception of this insect’s
sensory world. That was a limited view since mantids
also have sensitive hearing (Yager and Hoy, 1986, 1987,
1989; reviewed in Yager, 1999). They are the only
known terrestrial animals with a single ear. Not all
mantids hear, however, and even among the eared
there are several morphological and functional variations (Triblehorn and Yager, 2000; Yager, 1989, 1990,
1996a). The description that follows applies to the form
of auditory system anatomy and physiology that occurs
in approximately 65% of mantis species.
The mantis ear is located in the ventral midline of the
thorax near its junction with the abdomen . It comprises a deep longitudinal groove demarcated at its
anterior end by two prominent cuticular knobs. Ear size
does not increase proportionally with body size, e.g., a
25-mm mantis (Ameles heldreichi) has a groove 0.6 mm
long; an 85-mm mantis (Hierodula membranacea) has a
1.3-mm groove . Each groove wall contains an elongated, teardrop-shaped tympanum (Fig. 5B). The tympana face each other and are separated by only 100–200
µm. Because its walls are not parallel and the floor has
two large pits, the groove actually forms a long, thin
chamber of very complex shape that presumably has
correspondingly complex bioacoustic characteristics.
This anatomy dictates that the two tympana experience
identical pressure changes, hence the auditory system
lacks directionality (Yager and Hoy, 1989; Yager et al.,
1990). Neurophysiological recording coupled with ablations have further shown that the groove itself is an
integral part of the auditory system and provides a
5-dB gain in sensitivity, i.e., sensitivity is almost doubled
(Yager and Hoy, 1989). Combined with physiological
evidence that information from both tympanal organs
is immediately mixed in the CNS (Yager and Hoy,
1989), this provides a functional as well as anatomical
basis for viewing the mantis as an auditory cyclops.
The tympana are not typical of most insect ears in
that they are relatively thick (15–20 µm) and quite stiff.
A very large tracheal sac adheres tightly to the inner
surface of the tympanum. A tympanal organ containing
35–45 scolopidia is attached to each tympanum (Fig.
5C,D). Oddly, the attachment site is not near the center
of the tympanum, but rather at the extreme anterior
end where the tympanum is narrowest. Laser vibrometry has shown that even the narrowest portion has
high vibration velocities (Yager et al., unpublished
observations), but the biomechanics of this arrangement is not yet known.
Axons of the bipolar neurons of the tympanal organ
travel to the metathoracic ganglion in Nerve 7 (Yager
and Hoy, 1987; Yager and Scaffidi, 1993). The terminal
fields are several discrete, ipsilateral regions in the
metathoracic ganglion as well as in the first three
abdominal neuromeres (fused with the metathoracic
ganglion). Few, if any, of the mantid’s auditory fibers
terminate in mVAC as do those of other insects. All of
the terminal fields are near to the midline, and the
closest to the mVAC are near the supramedian commissure . We do not know the significance of this major
divergence from the established pattern, but it suggests
that the mantid’s CNS processing of auditory information may be different in some respects from that of other
insects. There are at least six bilateral pairs of interneurons that receive strong auditory input. A large, highly
symmetrical auditory interneuron (MR-501-T3) with
an axon ascending to the brain has been studied in
some detail (Yager and Hoy, 1989), and its serial
homologue in the mesothorax mediates low frequency
hearing in hymenopodid mantids (Yager, 1996a; see
below).
Mantis hearing is most acute at ultrasonic frequencies, generally between 25 and 50 kHz, and for most
mantids there is no appreciable sensitivity below 10
kHz. The lowest thresholds we have encountered were
20–30 dB SPL, although sensitivity for most species is
in the 40–60 dB SPL range and a few are less sensitive
at 65–75 dB SPL (Triblehorn and Yager, 2000; Yager,
unpublished observations). There is no physiological or
behavioral evidence to suggest that mantids can discriminate different frequencies (however, see below
concerning a two-eared mantis).
Mantids are unusual in that over 30% of the genera
show strong sexual dimorphism in the structure and
function of the auditory system (Yager, 1990). In these
cases, males have sensitive hearing and the ear anatomy
described above. If they can hear at all, the females
have auditory thresholds ⬎90 dB SPL. They have a
poorly developed metathoracic groove with tiny tympana and greatly reduced tympanal tracheal sacs.
Reduced hearing in females is uniformly associated
with shortened wings and the loss of flight ability. In
the few species where males have short wings, they too
have lost their auditory sensitivity.
Ultrasound triggers a complex, multi-component behavioral response after 50–100 ms in flying mantids.
The aerodynamic result is a steep, spiral power dive. In
both flight room and field studies, the response to
INSECT HEARING
387
Fig. 5. A: The single ear of praying mantids is located in a deep
groove (g) in the ventral midline between the metathoracic coxae
(mtc) as also indicated by the arrow in the upper drawing. In one
small lineage, a second, serially homologous midline ear has evolved
between the mesothoracic coxae (msc) that is tuned to 2–4 kHz rather
than ultrasound and operates independently of the metathoracic ear.
Scale bar ⫽ 1 mm. B: Transverse section through the metathoracic ear.
The tympana (ty) form the walls of the deep groove and are backed by
tracheal sacs (ts). Distinctive cuticular knobs (k) mark the anterior
end of the groove. Scale bar ⫽ 100 µm. C: A horizontal section through
the metathoracic ear; only the anterior-most portion is shown. The
tympanal organ (to) of 35–45 scolopidia attaches to the tympanum at
its extreme anterior end and is surrounded by haemolymph. Scale
bar ⫽ 100 µm. D: An enlargement of the medial end of the tympanal
organ showing three scolopales (s; rods and cap). The elongated nuclei
of the attachment cells (at) are visible in the lower left (toward the
tympanum); the nuclei at upper right are those of scolopale cells (sc)
and accessory cells. The attachment cells are associated with a long
ligament that actually connects the tympanal organ to the tympanum.
Scale bar: 10µm. A is reprinted from Yager DD. 1996a. Serially
homologous ears perform frequency range fractionation in the praying
mantis, Creobroter (Mantodea, Hymenopodidae). J Comp Physiol A.
178:463–475, with permission.
ultrasound successfully prevented capture by echolocating bats (Triblehorn, unpublished observations; Yager
and May, 1990; Yager et al., 1990).
Cockroaches (suborder Blattodea). Neurophysiological recording from a broad taxonomic sampling of
cockroaches (14 species from 4 of the 5 families) found
no evidence of hearing above 5 kHz or of a midline ear
as in mantids (Yager and Scaffidi, 1993). However,
Shaw (1994a,b) has shown that Periplaneta americana
can detect airborne sound below 5 kHz using the
subgenual organs (lowest mean threshold of 55 dB SPL
at 1.8 kHz; threshold rises steeply above 2 kHz). It has
long been known that the sensitivity of these tibial
chordotonal organs to mechanical vibration is exceptionally high (reviewed in Shaw, 1994a). However, cockroaches have no tympana on their legs, so a major
question is how the airborne sound can be coupled
effectively to the subgenual organs. Based on data
using isolated leg preparations, Shaw (1994b) suggested that the sound route is through the tracheal
system of the leg rather than directly through the
external cuticle or indirectly through ground vibra-
388
D.D. YAGER
Fig. 6. A: Dorsal view of a tiger beetle (Cicindela marutha) with
the elytra and wings spread to reveal the tympana (arrows) on the
dorsum of the first abdominal segment. Scale bar ⫽ 1 mm. B: A
generalized scarab like E. humilis to show the location of the ears
(arrows) just underneath the anterolateral edge of the pronotum.
C: An anterior view of the prothorax of E. humilis with the head
removed. The tympana are indicated by arrows; they are easily
distinguished from the surrounding neck membranes because of the
backing tracheal sacs. The location of the neck is indicated by the gray
oval (N). Scale bar ⫽ 1 mm. A is reproduced from Yager DD, Spangler
HG. 1995. Characterization of auditory afferents in the tiger beetle,
Cicindela marutha Dow. J Comp Physiol A 176:587–600, with permission of the publisher; B modified from Borror DJ, White RE. 1970. A
field guide to the insects. Boston and New York: Houghton Mifflin Co.
404 p; C modified from Forrest TG, Read MP, Farris HE, Hoy RR.
1997. A tympanal hearing organ in scarab beetles. J Exp Biol
200:601–606.
tions. The subgenual organs of all six legs show similar
responsiveness.
No behavioral function for P. americana’s sensitivity
to airborne sound has yet been discovered. However,
sound production in defensive contexts is well known
among cockroaches, and acoustic signals—probably
detected by the subgenual organs—play an important
role in social interactions in two genera, Nauphoeta and
Gromphadorhina, in one of the other cockroach families
(Hartman and Roth, 1967; Nelson, 1980; Nelson and
Fraser, 1980).
extensive destruction of other areas had only small
effects. The cuticle in the anterolateral corner is floppy
and membranous as opposed to the stiff cuticle of the
rest of the tympanum. Scanning electron microscopy
shows it to be finely ridged with a central invagination
or ‘‘dimple.’’ The vibration mechanics of the tiger beetle
tympana are not known.
Beneath each tympanum is a large tracheal air space
that is part of an extensive series of air sacs in the
abdomen and thorax. The tympanal air sac opens
externally through a greatly enlarged first abdominal
spiracle on the lateral body wall just below the tympanum.
The tympanal afferents travel in a branch (nsa1a) of
the dorsal root of the first abdominal ganglion. The only
nerve obviously associated with the tympanum is very
small branch that can be traced to the region just under
the anterolateral corner near the central invagination.
The tympanal organ itself has not been identified, but
hook electrode recordings from nsa1a suggest 4–20
auditory afferents (hence 4–20 scolopidia).
The auditory system of C. marutha is quite sharply
tuned to 30–35 kHz with lowest thresholds of 50–55 dB
SPL (Yager and Spangler, 1995). Many tiger beetles
occasionally produce stridulatory sounds at 30–35 kHz
when on the ground, but there is no behavioral evidence
of intraspecific communication (Pearson, 1988). In fact,
the ears are fully covered by the wings and elytra
except in flight, so the auditory sensitivity of potential
receivers on the ground may be very low. Ultrasound
does, however, trigger a complex multi-part behavior
Coleoptera
Tiger beetles (Cicindelidae). Spangler (1988b) uncovered the first evidence of hearing in this huge (350,000
species) insect order during field studies, and he confirmed that Cicindela lemniscata has sensitive ultrasonic hearing using a behavioral assay. A recent comparative study (Yager et al., 2000) has shown that
hearing is widespread in the very large, worldwide
genus Cicindela, but it is not universal in the family
Cicindelidae.
Ablation experiments localized two tympana to the
enlarged dorsal portion (tergum) of the first abdominal
segment (Fig. 6A). In species with low threshold hearing like C. lemniscata and C. marutha, the tympana are
thin and almost completely transparent except for their
medial portions. Selective ablations while recording
auditory responses neurophysiologically (Yager and
Spangler, 1995) showed that damage to a small triangular region 0.3–0.5 mm long in the anterolateral corner
of the tympanum raised thresholds by ⬎25 dB, but even
INSECT HEARING
with a latency of ⬍100 ms in flying beetles (Yager and
Spangler, 1997). A major component is the rapid and
powerful swing of the non-flapping elytra back into the
flapping hindwings. This deforms the hindwings—
presumably altering the aerodynamics—and at the
same time creates trains of loud ultrasonic clicks.
Arctiid moths, using a different mechanism, produce
acoustically similar click trains that effectively deter or
disrupt bat attacks (Acharya and Fenton, 1992; Dunning and Roeder, 1965).
Scarab beetles (Scarabidae). Behavioral observations in the field (Forrest et al., 1995) also led to the
discovery of paired hearing organs in one of the largest
beetle families, the Scarabidae (Forrest et al., 1997).
The currently known distribution of these ears is
limited to two tribes of one scarab subfamily, the
Dynastinae. Both phylogeny and anatomy make it clear
that hearing evolved independently in the Cicindelidae
and Scarabidae.
The ear of the scarab Euetheola humilis follows the
standard structural design for tympanate ears, but its
location is novel (Fig. 6B,C; Forrest et al., 1997). The
tympana are located dorsolaterally in the neck membranes just under the pronotal shield. The roughly oval
tympana are 1—2 mm in long dimension and 2–3 µm
thick. The structural contrast between the scarab tympanum and the surrounding tissue—cervical membrane that is 5 µm thick—is substantially less than in
other insects. A tracheal sac underlies each tympanum.
The location of the tympana offers these beetles the
possibility of controlling auditory sensitivity behaviorally. While walking or flying, the neck is extended, the
head is away from the pronotum, and the tympana are
exposed. When the head is retracted back to the pronotum, the tympana are covered and auditory responsiveness disappears (Forrest et al., 1997).
The tympanal organ of E. humilis comprises 4–8
chordotonal sensilla and attaches to the tympanum by
accessory (attachment) cells (Forrest et al., 1997). The
attachment site is not at the center, but at the dorsomedial apex of the membrane.
Both neurophysiological and behavioral audiograms
show that E. humilis is most sensitive to frequencies of
40–50 kHz with lowest thresholds of 55—60 dB (Forrest et al., 1995, 1997). Ultrasound triggers a stereotyped, lateralized response with a very short latency
(30–60 ms); a major component of the response is a
head roll. Although there is strong indirect evidence
that hearing helps scarabs evade echolocating bats as it
does in several other insects, their auditory behavior is
unique because it also occurs during walking. In all of
the other insects studies so far, complex, short-latency
evasive responses to ultrasound occur only when the
animal is flying. The response of E. humilis while
walking must afford protection from dangers other
than bats, since their auditory sensitivity is not high
enough to detect the approach of gleaning bats (Faure
et al., 1993).
Diptera. Based on behavior, hearing had been
suspected in some parasitoid flies since the mid-1970s
(Cade, 1975; Soper et al., 1976), but no one could have
anticipated just how unusual the fly ear would prove to
be when it was first described by Lakes-Harlan and
Heller (1992) and Robert et al. (1992). Similar, but
independently evolved, ears are found in parasitoid
389
flies in two dipteran families, Tachninidae and Sarcophagidae; most thoroughly studied are the ormiine
tachinids, Ormia ochracea (Robert et al., 1994, 1996a)
and Therobia leonidei (Lakes-Harlan and Heller, 1992).
The two tachinid ears are adjacent and essentially
fused in the ventral midline at the rostral end of the
prothorax, just behind the head (Fig. 7). A single large
airspace spanning both ears provides impedance matching for the two tympana. (Superficially, the ear looks
like a bubble under the fly’s ‘‘chin.’’) The ears are
sexually dimorphic, especially in size: the total width of
the two ears is 1.7 mm in females and 1.1 mm in males.
The attachment points of the two chordotonal organs
are separated by only 0.5–0.7 mm.
The female tympana are very complex, roughly triangular membranes that are only about 1 µm thick (Fig.
7A). They are radially corrugated with much finer
corrugations centrally than peripherally. A cuticular
bar (part of the intertympanal bridge) extends from the
midline toward the center of the tympanum. There is a
small invagination (tympanal pit) near the end of each
bar. The tympanal organ (‘‘bulba acoustica’’) is attached
anteriorly to the tympanum at the tympanal pit by way
of a thin, stiff apodeme and posteriorly by a ligament to
the wall of the tracheal space. Thus, both tympanal
organs span the rostral-caudal extent of the same
tracheal space.
Each of the ellipsoidal tympanal organs contains
longitudinally-oriented chordotonal sensilla of conventional structure. Although the ear anatomies of T.
leonidei and O. ochracea are largely the same, the
former has at least 200 sensilla in each bulba acoustica
as opposed to only 70 in the latter. The axons of the
bipolar sensory neurons join the frontal nerve and enter
the thoracic ganglionic complex where they have ipsilateral, medial terminations in all three thoracic neuromeres. The exact location of the auditory afferent
terminal fields in relation to the ganglionic tracts and
neuropiles is not as yet known. Stumpner and LakesHarlan (1996) have identified six bilaterally symmetrical pairs of auditory interneurons in T. leonidei, at least
three of which carry information to the brain.
Mantids and flies both have midline ears, but, nonetheless, have fundamentally different peripheral auditory designs. The mantis has a single ear in which two
tympana function together bioacoustically and two
tympanal organs pool their information in the CNS to
create a single ‘‘message’’ ascending to the brain. There
is a gain in sensitivity at the expense of directionality.
Despite their intimate adjacency, the two ears of the
tachinid fly nonetheless function separately and are
thus able to provide directional information. This should
not be possible given any of the known mechanisms for
directional hearing (Michelsen, 1998), and, in fact,
these small insects use a unique and previously unknown mechanism.
Miles et al. (1995) and Robert et al. (1996b, 1998)
have used laser vibrometry, experimental manipulation, and mechanical modeling to discover and describe
the directional mechanism (Fig. 7C). The key feature is
mechanical coupling between the two tympana. The
intertympanal bridge comprises the two cuticular bars—
with the tympanal organ attachments at their ends—
connected at a midline pivot point. The bridge links
together the motion of the two tympana in the manner
390
D.D. YAGER
Fig. 7. A: Scanning electron micrograph of the prothoracic ear of
the tachinid fly Ormia ochracea; the head has been removed. The
white arrowheads indicate the boundaries of the tympanum. The
tympanal pit (tp) is evident at the end of each half of the intertympanal bridge. Two levels of striations radiate from the end of the bridge:
medially the striations are very fine and laterally they are more widely
spaced. Scale bar ⫽ 200 µm. B: A generalized tachinid fly (wings and
distal legs removed) indicating the location of the ears beneath the fly’s
‘‘chin.’’ C: A schematic representation of the mechanical model to
explain the novel mechanism for directional hearing in ormiine
tachinid flies. Force and subsequent movement at the tympanal pits
(arrows) causes the intertympanal bridge (long rectangles) to move
around its fulcrum (F) in the midline. The diamonds (D) represent a
combination of restoring force and delay. The connection between the
tympanal pits and anchor points (A) is the tympanal organ and its
ligaments. The lower drawing shows the relative motion of the two
halves of the intertympanal bridge in response to sound coming from
the left. Contralateral movement is in the opposite direction and has a
lower amplitude than ipsilateral movement; it is also delayed by 50–60
µs (not shown). See text for further explanation. A modified from
Robert et al. (1994); B modified from Colless and McAlpine (1991);
rCSIRO); C redrawn from Robert and Hoy (1998).
of a flexible lever with a spring-like restoring force
acting at each end. If the intertympanal bridge were a
single rigid bar, an inward motion of the tympanum on
one side would cause a simultaneous outward motion of
equal amplitude on the other. However, the bridge
actually comprises two bars with a non-rigid linkage
that introduces damping and a time delay to the
contralateral motion. The interaural intensity differ-
ence for a 5 kHz lateral sound source is 0 dB and the
interaural time delay is 1–2 µs, neither of which are
detectable by insect neural systems. As a result of the
intertympanal coupling, tympanal vibration contralateral to the sound source is delayed by 50–60 µs and has
10–15 dB lower amplitude than the ipsilateral vibration. Recordings from the auditory afferents reveal a
further delay amplification (the source is not clear) so
INSECT HEARING
that the ipsilateral response leads the contralateral by
approximately 320 µs, a delay long enough to be used by
the CNS for directional processing. Miles et al. (1995)
developed a mathematical model of the mechanical
system whose predictions matched the measured tympanal vibrations in response to sound and to mechanical displacement very closely.
Female ormiine tachinid flies orient accurately to a
sound source and use this capability to locate hosts for
their offspring. For O. ochracea, these are male field
crickets (Robert et al., 1992); the European T. leonidei
seeks out male bushcrickets (Lakes-Harlan and Heller,
1992). The optimal frequencies for tympanal vibration
match the dominant calling song frequencies of the
hosts: 5 kHz for O. ochracea and 30–40 kHz for T.
leonidei. The parasitoid sarcophagids have not been
studied in detail, but also appear to orient preferentially toward the dominant calling song frequencies of
their hosts (cicadas; Soper et al., 1976). Once the female
locates a singing male, she deposits first instar larvae
on or near the host. The larvae burrow into the male
where they feed and grow. Parasitization rates in a host
population can be over 50% of the males (Lakes-Harlan
and Heller, 1992; females are never hosts). Male ormiine flies have smaller ears than females. The functional
consequence for O. ochracea is a lower auditory sensitivity by 40–50 dB and tuning to ⱖ10 kHz. The behavioral
role of hearing in males is not known.
Some Tympanate Groups Revisited
Many notable studies since 1985 have extended our
knowledge of auditory anatomy, physiology and behavior in the ‘‘traditional’’ tympanate insects systems.
These are discussed in a recent review volume (Hoy et
al., 1998). I have selected three of the newest examples
that have particular relevance to a discussion of insect
ear evolution.
Multi-Eared Grasshoppers. The South African
pneumorid grasshopper Bullacris membracioides has
an acoustic communication system in which males
produce loud calls that are answered by the approaching females (van Staaden and Römer, 1997). After a
characteristic acoustic duet, the male moves toward the
female and mating ensues. Females can detect the male
call at distances up to 2 km because the male call is loud
(98 dB SPL at 1 m) and because female hearing is
among the most sensitive of all insects (van Staaden
and Römer, 1997). Thus, it is somewhat surprising to
discover that these insects lack differentiated tympana,
and even more surprising to find that they have six
serially homologous pairs of functional auditory organs
in their abdomen (van Staaden and Römer, 1998).
The ‘‘ear’’ in the first abdominal segment (A1) is
located in the lateral (pleural) region and is clearly
homologous with the more conventional ears of other
locusts and grasshoppers (Meier and Reichert, 1990).
The number of chordotonal sensilla in the tympanal
organ is huge—almost 2,000; other chaeliferans have
70–100. The tympanal organ is attached to the lateral
body wall by two unusually long bundles of attachment
cells, each associated with its own group of scolopidia.
Physiological recording from the afferents show lowest
thresholds of 10–15 dB SPL at a best frequency of 4 kHz
(mismatched to the dominant frequency of the male’s
call, 1.7 kHz).
391
The next five abdominal segments (A2–A6) have
serially homologous auditory organs. Although structurally similar to the A1 ear, these are smaller with only 11
sensilla each. They are tuned to 1.5–2.0 kHz, and the
sensitivity decreases systematically in progressively
caudal segments (thresholds of 58 dB SPL in A2 to 77
dB SPL in A6).
Strategic ablations combined with playback experiments to assess behavior have demonstrated that the
physiological intensity range fractionation afforded by
the six pairs of auditory organs has its counterpart in a
graded series of behavioral responses that are important for successful reproductive encounters (van Staaden
and Römer, 1998).
Ears on Wings. Although the tiny tympanate ears
on the radial vein of green lacewing (Neuroptera)
forewings have been studied in some detail (reviewed in
Miller, 1984), the wing ears of Lepidoptera have not
received equivalent attention. Early anatomical studies
(Bourgogne, 1951; Vogel, 1912) identified ‘‘Vogel’s organ,’’ an ear-like structure with a chordotonal organ
(12–40 scolopidia) at the base of the wings in some
nymphalid butterflies (a family within the superfamily
Papilionoidea, the ‘‘true butterflies’’; Scoble, 1995). Using neural recording and a startle behavior, Swihart
(1967) found evidence for functional auditory organs in
two nymphalid subfamilies, Heliconiinae and Limenitidinae. Ear structure was similar in both subfamilies as
was the sensitivity (60–65 dB SPL at the best frequency, 1.2 kHz). However, the heliconiine ears were
localized to the hindwings, whereas ears in the Limenitidinae are on the forewings. Ribaric and Gogala (1996)
have confirmed hearing in a third nymphalid subfamily
(the Satyrinae; ears on forewings). A number of limenitidiine species produce loud clicks during social interactions (Swihart, 1967).
Alar ears have recently been discovered in a second
butterfly superfamily, the Hedyloidea. The initial tentative identification based on gross anatomy (Scoble,
1986) has now been confirmed and refined with histological and behavioral studies (Yack, personal communication). The ears are at the base of the forewings and
appear the be built of structures homologous to Vogel’s
organ in nymphalids. Hedylid butterflies are nocturnal,
and they respond in flight to ultrasound with typical
evasive behaviors.
The evolutionary relationships of the various butterfly wing-ears is a puzzle, in part because the phylogeny
is unsettled. Parsimony suggests at least two independent evolutions, and there is ample precedent for
repeated appearance of ears at the same body location
in a lineage (see below). However, some anatomical
features point to a common origin for alar ears in the
two butterfly superfamilies (Yack, personal communication).
Ears on Mouth Parts. Roeder and colleagues
(Roeder et al., 1970; Roeder, 1972; Roeder and Treat,
1970) found a unique auditory organ sensitive to ultrasound built into the mouth parts of species in one tribe
of hawkmoths (Choerocampini, Macroglossinae, Sphingidae; Fig. 8A). Sensitivity was 40–45 dB SPL at 25–35
kHz, and audition was presumed to aid bat evasion.
Göpfert and Wasserthal (1999a,b) have extended the
story by providing new behavioral and physiological
information on choerocampine hearing and have also
392
D.D. YAGER
Fig. 8. A: The ears of choerocampiine and acherontiine hawkmoths are located in the mouth region (arrow). B: Dorsal view of the
head of a choerocampiine hawkmoth. The labral pilifers lie just lateral
to the proboscis (pr) and medial to the labial palps (pa); the palps are
medial to the compound eyes (e). The left palp is moved laterally out of
its normal position. The right palp is drawn in horizontal section
showing that the interior is primarily air space. In their normal
positions, the distal tip of the pilifer just touches the medial face of the
palp, i.e., the tympanum. C: Frontal scanning electron micrographs of
an acherontiine hawkmoth, Acherontia atropos. Left: Left palp is
deflected laterally to expose the pilifer. Right: Dorsal close-up view of
the left palp-pilifer in their normal positions. The pilifer contacts the
dorsal surface of the palpal scale plate (sp) and moved dorsoventrally
when the scale plate vibrates. The hinge is visible as a crease at the
base of the pilifer. Scale bars ⫽ 1 mm. A modified from O’Toole C,
editor. 1986. The encyclopedia of insects. New York: Facts On File
Publications. 152 p; B redrawn from Roeder et al, 1970. C modified
from Göpfert MC, Wasserthal LT. 1999a. Hearing with the mouthparts: behavioral responses and the structural basis of ultrasound
perception in acherontiine hawkmoths. J Exp Biol 202:909–918.
added a fascinating anatomical and evolutionary twist
with the discovery of mouth-ears in the Death’s Head
moth (Acherontia atropos) and some of its relatives,
members of a different hawkmoth lineage (Acherontini,
Sphinginae, Sphingidae).
In both sphingid groups, the two ears are located
near the midline on each side of the proboscis (Fig.
8B,C). They have two disjoint parts: a more lateral
labial palp that is specialized to increase sensitivity to
airborne sound, and a medial labral pilifer modified for
efficient transduction. In the choerocampines, the second segment of the palp is like a balloon. It is enlarged
(1.0–1.5 mm across), filled with air, and has thinned
cuticle, especially its medial wall, which is also devoid
of scales (Fig. 8B). The pilifer has two lobes; the distal
lobe is normally in close contact with the smooth medial
surface of the palp. The pilifer is 0.2–0.3 mm long.
Laser vibrometry shows that the medial face of the palp
is the tympanum; other areas of the palp do not vibrate
significantly in response to sound. The pilifer is a bit
like the tonearm on a record player: the distal tip
touches the tympanum and transmits the vibration to a
single chordotonal sensillum located at the base of the
pilifer.
The auditory organ is quite different in acherontine
hawkmoths (Fig. 8C). The palp is not enlarged and does
not have thinned cuticle. However, its medial face is
deeply concave, and a tuft of broadened scales forms a
‘‘plate’’ protruding into the concavity. The scale plate’s
surface area is approximately 1 mm2. The pilifer has a
single lobe, it is elongated (0.6–0.8 mm), and it is
hinged at its base. In contrast to the choerocampines,
the scale plate rather than the medial wall of the palp
vibrates in response to airborne sound. Thus, there is
no tympanum in any conventional sense. The pilifer
has broad contact with the scale plate and rocks
dorsoventrally around the hinge when the scale plate
vibrates; this stimulates the single scolopidium at the
base of the pilifer.
Both acherontine and choerocampine hawkmoths are
sensitive only to ultrasound, generally at 20–40 kHz
although a few species are tuned to 50–70 kHz. Göpfert
and Wasserthal (1999a,b) found physiological thresholds of 50–55 dB SPL and behavioral thresholds 10–15
INSECT HEARING
dB higher. They identified several ultrasound-triggered
behaviors including some during tethered flight that
are consistent with bat evasion.
Even though the ears are built of homologous parts,
the phylogeny, the divergent anatomy, and the different
sound-transducing devices all point to independent
evolutions of hearing in the choerocampine and acherontine hawkmoths.
EVOLUTION OF INSECT EARS
In no other animal class has an exteroceptive sense
with specialized peripheral organs evolved independently as many times as hearing has in the Insecta. The
number of known independent innovations of insect
ears is currently at 19 and climbing. By virtue of this
diversity, insect audition provides a unique opportunity
to study the evolution of new sensory systems. In other
words, how does an animal go from earless to eared?
Are there particular peripheral precursors present in
all insects? What determines where on the body the
ears appear? What genetic or epigenetic processes
govern the transformation? What changes must occur
in the CNS to process input from the new sensory
modality? How do acoustically-triggered adaptive behaviors arise?
Ultimately evolution comes about by changes in
developmental processes or their timing. Therefore, it
makes sense to consider auditory development in the
discussion of insect ear evolution. Boyan (1998) provides an extensive review of insect auditory system
development.
Why?
Superficially, this question of ultimate causation has
straightforward answers. Since we know the current
functions of hearing in insects, we infer that the
selective forces leading to hearing in different groups
were the need to avoid predators, the need to attract
and select appropriate mates, and the need of parasitoids to find hosts for their offspring (Bailey, 1991). The
problem is that current function need not be the same
as the original function.
Except for a few orthopterans (Carpenter, 1992), the
fossil record of ears is very scant and provides little
help. Comparative studies of both anatomy and acoustic behavior have, however, provided some strong clues.
For instance, some moths use intraspecific acoustic
communication in courtship, but it is widely accepted
that this is a recent adoption of ultrasonic hearing and
sound production originally in place as defense mechanisms against bat predation (Fullard, 1998; Sanderford
and Conner, 1990). Comparative and neuroanatomical
studies yield the same conclusion for locusts and grasshoppers (Otte, 1977; Reide et al., 1990). For the ensiferans, however, the historical pattern is probably reversed. Both fossil tegmena that appear highly
specialized for sound production and legs with tibial
ears are known that predate the appearance of echolocating bats (65–85 million years ago; Novacek, 1985) by
at least 100 million years (Carpenter, 1992). Thus,
ultrasonic hearing for defense seems to be a recent
additional function to an ancient acoustic intraspecific
communication system (Hoy, 1992).
The growing comparative literature on insect ears
suggests that secondary loss of the auditory system is a
393
common and important evolutionary pattern among
tympanate insects. There are examples among katydids (Gwynne, 1995), moths (Scoble, 1995), grasshoppers (Mason, 1968), and crickets (Gwynne, 1995; Otte,
1990). It has probably occurred five times among the
North American tiger beetles of the genus Cicindela
(Yager et al., 2000), and no fewer the 14 times among
the praying mantids (Yager, 1990). It is often, but not
always, associated with auditory sexual dimorphism in
which males hear and the females do not. There is also
an extremely tight correlation of secondary ear loss
with the secondary loss of flight (wing reduction or
absence) in species that use hearing to evade bats (the
exceptions are insects like crickets that also use acoustic intraspecific communication; Otte, 1990). The ‘‘Why?’’
in sexually dimorphic cases has an appealingly plausible answer: studies in several insect groups show that
under certain ecological conditions, females can profitably ‘‘trade’’ flight for increased fecundity (Roff, 1986;
Wagner and Liebherr, 1992; Zera et al., 1997). Flightless animals face no pressure from echolocating bats—
the auditory system becomes a needless expense and
disappears.
When?
In terms of absolute time, the absence of fossil ears
poses the same problems noted above; Carpenter (1992)
provides the best review. Specialized stridulatory structures were widespread in the Orthoptera by the Triassic, and tibial ears are present in some Haglidae (an
ensiferan) from that period. Tympana on the first
abdominal segment of Eocene locusts are known, but
there is molecular and comparative evidence suggesting that pneumorid stridulation (and ears?) dates to the
Jurassic (van Staaden and Römer, 1998). Cicadas had
specialized tymbals by the Paleocene.
It is easier to deal with phylogenetic age, which can
often be inferred from the results of comparative studies superimposed on hypothesized phylogenetic trees.
For instance, it is clear that hearing appeared very
early in the history of both of the two major orthopteran
suborders (although after they had diverged, of course;
Gwynne, 1995; Otte, 1977; Reide, 1987). This is also the
case for the metathoracic mantis ear (Yager, 1989, 1990;
however, the mesothoracic ear of hymenopodid mantids
appeared very late; Yager, 1996a). At the other extreme,
tachinid and sarcophagid fly ears are phylogenetically
very recent innovations in their respective lineages
(Edgecombe et al., 1995).
How?
What are the proximate mechanisms that bring
about the transition from earless to eared? How is the
normal pattern of development changed to yield an
auditory organ composed of several tissue types organized into a structure that transduces airborne sound
first into mechanical vibration and then into neural
signals?
Precursors. 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-
394
D.D. YAGER
Fig. 9. Schematic drawing of the embryonic organization of chordotonal organs in the body wall of a locust. The tympanal organ (to) in
the lateral wall of the first abdominal segment (A1) is represented in
the other abdominal segments by its serial homologues, the pleural
chordotonal organs (pco). In the mesothorax (T2) and metathorax
(T3) the serial homologues of the tympanal organ are the wing hinge
chordotonal organs (wco); these are associated with a multipolar
stretch receptor (sr). The stereotyped organization of the body wall
chordotonal organs into three groups persists with some modification
into adulthood. It is also seen in Drosophila and is probably an
organizing feature for all insects. Modified from Meier T, Reichert H.
1990. Embryonic development and evolutionary origin of the orthopteran auditory organs. J Neurobiol 21:592–610..
ten in small clusters—are numerous and widespread
throughout the bodies of all insects (Field and Matheson, 1998; McIver, 1985). Slifer (1936) counted 76 pairs
of chordotonal organs in a grasshopper.
Anatomical studies comparing tympanate insects
with closely related, but atympanate species have
identified tympanal organ precursors in several taxa.
Based on location, structure, and innervation pattern,
Yack and Fullard (1990) established the homology
between the tympanal chordotonal organ in a noctuid
moth and a similar organ in an atympanate saturniid
moth. They used neurophysiological recording to show
that the chordotonal homologue of the saturniid responds to elevation or depression of the hindwing, and
apparently functions as a proprioceptor at the wing
hinge. Yager and Scaffidi (1993) identified the homologue to the mantis tympanal organ in cockroaches as
well as the serial homologue in the atympanate mesothoracic segment of the mantis. The precursor is almost
identical in structure and neuron number, but differs
from the tympanal organ in the geometry of its attachments. In this case, behavioral experiments (Yager and
Tola, 1994) suggest that the precursor is an extremely
sensitive vibration detector, and there is further evidence linking its vibration sensitivity to a non-cercal
escape system in the cockroach (Pollack et al., 1994).
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 (Kalmring et al., 1994; 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 (⬍40 vs. 70). Its function is unknown,
although it is most likely a proprioceptor.
The most potent demonstration of tympanal organ
precursors comes from developmental studies. Meier
and Reichert (1990) used neuron-specific antibodies to
trace the embryonic development of the locust tympanal organ on the lateral wall of the first abdominal
segment (Fig. 9). The tympanal chordotonal organ is
formed at approximately 40% of embryonic development by invagination of the body wall near the posterior border of the segment. From the outset, the organ
has its adult number of 70–90 sensory neurons. The
pleural chordotonal organs form at the same developmental time, by the same process, and at the homologous locations in the other pregenital abdominal segments. Cell migration and growth of the afferent nerve
are largely identical for the two organ types, but the
pleural chordotonal organs have only 10–15 sensory
neurons. By comparison, they found that an earless
grasshopper forms a normal pleural chordotonal organ
in the first abdominal segment. Thus, it is clear that the
chaeliferan ear derives from the pleural chordotonal
organ of the first abdominal segment and that it has
serial homologues throughout the thorax and abdomen.
Pleural chordotonal organs appear to monitor respiratory movements (Hustert, 1975; Orchard, 1975).
Using the same developmental techniques, Meier
and Reichert (1990) also showed that the crista acoustica in the prothoracic leg of bushcrickets derives from a
linear array of mechanoreceptors associated with the
subgenual organ. There are unspecialized serial homologues in the other pairs of legs, and they found that the
‘‘crista acoustica’’ in the prothoracic leg of an atympanate species was unspecialized like the organ in the
mesothoracic and metathoracic legs. Not all of the
sensory neurons are present initially, but the number
increases with development. The adult crista acoustica
has 30–40 sensilla; the serial homologues have 10–15.
An especially intriguing finding was that the linear
array of sensilla reflecting a tonotopic organization in
adults is present even when the receptors first appear
in the embryo.
Lewis and Fullard (1996) looked at development of
the noctuoid moth tympanal organ across metamorphosis. They showed that the tympanal organ does not
develop de novo during metamorphosis, but, rather, is
the post-metamorphic derivative of a proprioceptor
present in the larvae. In contrast to most other cases,
the adult tympanal organ has fewer rather than more
chordotonal sensilla than its precursor (2 vs. 3; this is
INSECT HEARING
true both compared to the larval precursor and to the
homologue in an atympanate moth).
The pneumorid grasshoppers provide an especially
interesting and complementary perspective on tympanal organ precursors. Because of their phylogenetic
position among the chaelifera and because of the homology of the pneumorid auditory organs with other chaeliferan ears, van Staaden and Römer (1998) argue that
the atympanate, but highly sensitive, serially homologous auditory organs of pneumorids represent a transitional form between the pleural chordotonal organ
precursors and fully tympanate auditory systems.
In summary, the tympanal organs of all tympanate
insects studied have chordotonal precursors and have
not arisen de novo. Tympanal organs have many more
sensilla than their precursors except in mantids (the
same) and noctuoid moths (fewer). Some of the precursors are proprioceptors monitoring slow body movements. The normal function of others seems to be
indirectly exteroceptive by picking up substrate (and/or
air?) vibrations transmitted through cuticle.
Determinants of Body Location. Although the
diversity of ear locations on the insect body may seem
unpatterned and almost random, recent comparative
and developmental studies have opened the way for a
simpler and more orderly view. Raff (1996) provides a
superb examination of these concepts that guide the
rediscovered field of ‘‘evolutionary developmental biology’’; Kutsch and Breidbach (1994) provide a related
discussion focusing on invertebrates. For the evolution
of insect ears, the key lies in ‘‘modularity,’’ not only the
modular construction of the insect body, but the underlying modularity of developmental processes. There is
also a hierarchy of modules. For example: the insect
body is constructed of a series of repeated modules
(body segments); within each of the three thoracic
segments, a modular unit of gene expression and
induction directs the formation of a leg on both sides;
within each leg module there are separate anterior,
posterior, distal, and proximal modular processes (Tabin,
1991). Thus, the same developmental module in different body segments produces serially homologous components; in this sense, serial homologues are the same
structure (Haszprunar, 1992; Wagner, 1989).
The duplication process—multiple segments built by
the same sequence of gene expression and induction—is
often accompanied by divergence, alteration through
natural selection of some modules of particular body
segments (Raff, 1996). For instance, the prothoracic
legs of mole crickets are specialized for digging and are
quite different in structural detail (but not fundamental design) from the serially homologous walking legs.
The most conserved elements among body segments are
the CNS and the peripheral innervation patterns (Dumont and Robertson, 1986; Meier et al., 1991; Thomas
et al., 1984). Thus, even in the highly fused ganglionic
mass of the moth thorax, the segmental, modular CNS
architecture is preserved (Boyan and Ball, 1993; Boyan
et al., 1990). A more extreme example: even though the
adult anatomies are radically different, the serial homology of insect mouth parts and legs is obvious in the
remarkable similarity of their sensory innervation patterns during development (Meier and Reichert, 1991).
With these concepts in mind, it is interesting to look
at ears in three different orders and located at three
395
different sites on the body: locusts (lateral A1), tiger
beetles (dorsal A1), and noctuid moths (dorsal/caudal
T3). Yager and Spangler (1995) argued that a major
difference in body configuration obscures the fact that
the ears of locusts and tiger beetles are built from
homologous parts, with the pleural chordotonal organ
as precursor of the tympanal organ in both cases.
Evidence from embryology (Meier and Reichert, 1990)
and genetics (Bier et al., 1990) has demonstrated the
serial homology of the abdominal pleural chordotonal
organs with the thoracic wing hinge chordotonal organs
(Fig. 9). Yack and Fullard (1990) have convincingly
shown that the wing chordotonal organ in T3 is the
precursor of the noctuid tympanal organ. Finally, there
is substantial evidence that the moth and locust wing
hinge chordotonal organs are homologous (Wilson and
Gettrup, 1963; Yack, 1992; Yack and Roots, 1992).
Following this chain of logic, three anatomically different ears in unrelated taxa are nonetheless closely allied
in an evolutionary/developmental sense. These three
independent ear evolutions form an ‘‘auditory cluster’’
that may additionally count among its members the
little-studied auditory systems of some aquatic hemipterans (on lateral mesothoracic and metathoracic segments; Prager, 1976) and uraniid moths (on lateral A2;
Scoble, 1995) Other auditory clusters may include
mantids/tachinid flies (mid-ventral) and cicadas/pyralid
moths/geometrid moths (ventrolateral). A more surprising—and speculative—cluster would be based on the
serial homology of insect mouth parts with the legs
(Meier and Reichert, 1991); it would include sphingid
moths and the ensiferans. Finally, the several occurrences of wing ears would form a separate cluster
(complicated, however, by the growing evidence that
wings are derived from legs and share the same developmental patterns, although some of the genes differ;
Williams and Carroll, 1993).
There are two especially notable examples that reinforce the segmental equivalence of ear locations and its
potentials. Without doubt, the most striking case is the
six serially homologous pairs of auditory organs found
in the abdominal segments of pneumorid grasshoppers
(described above; van Staaden and Römer, 1998). In
this instance, the auditory information from all the ears
seems to be integrated in service of the same behaviors,
mate attraction and courtship. Second, mantids in the
hymenopodid subfamilies Hymenopodinae and Acromantinae have two ears (an ‘‘auditory bicyclops’’; Yager,
1996a). One of these is in the metathoracic midline and
has the characteristics described above for other mantids. The second is a serially homologous ear in the
mesothorax that has equal or greater sensitivity, is
tuned to 2–4 kHz rather than ultrasound, functions
independently of the metathoracic ear, and mediates
different behaviors. In essence, these insects have
evolved two separate auditory systems. In an odd way,
pneumorid grasshoppers and hymenopodid mantids
are their own auditory clusters.
A corollary to the ‘‘auditory cluster’’ hypothesis is that
there are locations on the insect body that are especially likely sites for the appearance of an ear. The
limiting determinant is most likely the presence of a
neural precursor to the tympanal organ rather than
availability of a trachea for the tympanal air sac or
suitable cuticle for the tympanum itself. Chordotonal
396
D.D. YAGER
organs are numerous and found throughout the body,
but they are not evenly distributed. Embryological
studies clearly show a stereotyped pattern of three
chordotonal organ groups (ventral, lateral, and dorsal)
in each thoracic and abdominal body segment (Fig. 9). A
remarkably similar pattern is found in locusts and in
Drosophila (Ghysen et al., 1986; Meier et al., 1991) and,
judging by adult anatomy (Finlayson, 1976) and phylogenetic history (Carpenter, 1992), is shared by most, if
not all insects. The embryological distribution persists
in the adult with two modifications that are also
common to most species across a broad taxonomic span
(a compilation is provided in Finlayson, 1976). The
dorsal group often does not persist in the adult as a
chordotonal organ; it may be the precursor of multipolar stretch receptors found in each segment (Heathcote,
1981; Meier et al., 1991). The ventral group typically
gives rise to separate ventromedial (proximal) and
ventrolateral (distal) COs (Finlayson, 1976; Meier et
al., 1991). There can be further subdivision and elaboration, especially of the ventromedial group. Slifer (1936)
found four ventromedial COs with a total of 72 scolopidia in a grasshopper rather than the 1—2 COs (6—10
scolopidia) present during development (Meier et al.,
1991).
The distribution of chordotonal organs in adult insects predicts three ‘‘hot spots’’—ventromedial, ventrolateral, and lateral—and those locations correspond to
the observed auditory clusters of species with ears
located on the body.
Why a particular insect bases its ear location on one
chordotonal organ group and not another may have less
to do with availability of ear precursors than it does
with constraints imposed by the animal’s natural history and anatomical specializations. Considering relatively homogeneous lineages, ears have evolved twice
among the parasitoid flies and twice among sphingid
moths, in both cases at the same location (other examples are the midline ears of mantids and the alar
ears of butterflies). As a counterexample, scarab beetles
and tiger beetles have vary different ecologies and body
shapes, and ears that appeared in different locations.
The lateral and ventrolateral groups in segments T2-A2
are by far the most common precursors possibly because those locations maximize availability of directional cues and at the same time afford protection for
the tympana. An indirect flight mechanism and a
shortened abdomen might dictate that the dipteran ear
could not use the lateral and ventrolateral body wall
CO groups, and therefore a ventromedial location became most practical. All other things being functionally
equal, simple fortuity may also be a sufficient explanation.
Earless-to-Eared Transition. The central question in the evolution of insect auditory systems—What
changes in developmental programs lead to the evolutionary transition from earless to eared?—remains
unanswered. The tools for uncovering the answer will
come from molecular genetics and evolutionary developmental biology. The genetic and molecular control of
chordotonal organ development is now understood in
considerable detail for Drosophila (Hartenstein, 1988;
Jan and Jan, 1994; Okabe and Okano, 1997). For
instance, certain mutations of the engrailed gene lead
to absence of the pleural chordotonal organs without
affecting any other sensory structures in the region
(Hartenstein, 1987). The serial homology of abdominal
pleural COs and the thoracic wing hinge COs (Fig. 9)
has been confirmed using a mutant of the rhomboid
gene that can change the segmental specification of a
pleural CO from abdominal (five scolopidia) to thoracic
(three scolopidia; Bier et al., 1990). More recently the
induction of chordotonal organ precursors by sequential action of the genes atonal, rhomboid, and argos has
been described (Okabe and Okano, 1997). It is especially interesting from the evolutionary perspective
that the proneural gene atonal directs the formation of
chordotonal organs in Drosophila (Jarman et al., 1995)
and that the mouse homologue of atonal (Math1) is
necessary for the genesis of hair cells in the inner ear
(Bermingham et al., 1999). Although nothing is yet
known about the genetic control of tympanal organ
development in any insect, the information from Drosophila clearly provides a strong groundwork.
The evolution of insect ears involves more than just
the chordotonal organs. At minimum, some process or
processes should: (1) trigger the increase in sensory
neuron number compared to the chordotonal precursor
that is seen in most, but not all, tympanate insects; (2)
trigger thinning of a region of cuticle or enlargement of
an existing patch of membranous cuticle; (3) trigger
enlargement of a nearby trachea or migration of an
existing tracheal sac to the tympanum; and (4) trigger a
reorientation of the three ear components so that they
are in the proper spatial relationship to one another.
The ontogenetic transition from earless to eared
takes place in stages that may provide clues to the
evolutionary processes. In every hemimetabolous insect studied, the neural components of the ear are in
place at hatching, although there may be some reorientation postembryonically as nearby structures mature
(Klose, 1991; Meier and Reichert, 1990; Rössler, 1992;
Yager, 1996b). Nonetheless, the youngest nymphs do
not hear. A later, second stage of auditory development
builds the tympanum and brings an impedancematching tracheal sac into apposition with it. For
crickets, the appearance of auditory function is abrupt.
Last instar nymphs have no appreciable sensitivity; the
tympanum appears at the imaginal molt and with it
come low thresholds (Ball and Hill, 1978). For tettigoniids (Rössler, 1992), locusts (Petersen et al., 1982), and
praying mantids (Yager, 1996b), the transition is more
gradual. For instance, mantids first have detectable
auditory sensitivity about half way through nymphal
development, and it increases with each successive
instar. The progressively lowering thresholds parallel
the enlargement and thinning of the tympanum and
the formation of the tympanal tracheal sac. Fully adult
ear structure and sensitivity appear at the last molt.
Harron and Yager (1996) have shown that the second
stage of ear development can be selectively disrupted
by appropriately timed doses of juvenile hormone; the
outcome is deaf and short-winged, but otherwise normal adults.
Looking Ahead
Based on the discussions above, there are some
generalizations that can help guide the search for
developmental and evolutionary processes in insect
audition:
397
INSECT HEARING
● Ears and auditory systems have not arisen de novo,
and we can focus on changes in the development of
known precursors.
● We do not need to look for 19 different evolutionary/
developmental mechanisms. The ideas underlying
auditory clusters suggest at most 5–6 mechanisms.
If, as seems probable, the different body wall chordotonal organ groups have parallel developmental
processes, the number may go down to three: body,
wing, and leg.
● The number could be one. There may be an interesting parallel with the study of eye evolution in metazoans. Anatomically-based phylogenetic studies suggested at least 15 independent evolutions of lensed
eyes and 40–65 appearances of photoreceptors in six
metazoan phyla (Salvini-Plawen and Mayr, 1977).
However, the discovery of a ‘‘master control gene’’
(eyeless and its homologue Pax-6) triggering a highly
homologous gene cascade determining eye morphogenesis in both vertebrates and invertebrates argues
strongly for a common developmental origin (reviewed in Halder et al., 1995a). The haunting image
of fruit flies with fully differentiated compound eyes
on their legs or wings or antennae due to local
expression of the eyeless gene (Halder et al., 1995b)
inevitably raises the prospect that there may be a
corresponding control gene that when turned on,
orchestrates the construction of an insect ear, regardless of position on the body.
● Anatomical changes in the central nervous system to
accommodate audition are likely to be small compared to those in the periphery. The idea that the
CNS is far less plastic than the periphery has
emerged as a general principle in invertebrate neurobiology (Boyan and Ball, 1993; Dumont and Robertson, 1986). We know, for instance, that each insect
auditory system uses the same mechanoreceptive
region (mVAC) of CNS neuropile regardless of the
location of the ear or the nerve root carrying the
auditory information (discussed above). Yager and
Hoy (1989) argued that the most prominent auditory
interneuron in mantids (MR-501-T3) is the homologue of a well-studied auditory interneuron in locusts (531; also called ‘‘B1’’), as well as of a nearly
identical cell (DPG 502) in cockroaches shown by
Ritzmann et al. (1991) to receive vibratory input
from the subgenual organs. The implication is that
both mVAC and MR-501-T3/531/DPG 502 are components of an ancient chordotonal mechanoreceptive
system that has been coopted repeatedly for audition
(Boyan, 1993).
This does not, however, mean that the auditory CNS
is devoid of interest. On the contrary, one of the most
important unanswered questions about the evolution of
insect auditory systems concerns CNS changes. With
the advent of hearing, portions of the CNS that had
processed proprioceptive information begin receiving
exteroceptive information that has a different meaning
to the animal and must trigger different behavioral
responses. How does the CNS reinterpret the afferent
information and link it to appropriate behaviors? While
there may not be gross anatomical change, clearly some
rewiring is necessary. Least likely is the creation of
entirely new circuitry and entirely new behaviors.
Evolution most often builds from existing structures,
and just as there are anatomical tympanal organ
precursors, there are certainly precursor neural circuits and behaviors (Dumont and Robertson, 1986). At
the other extreme, CNS circuitry and behavior may be
entirely modular so that the only change required to
accommodate hearing is to disconnect the input from its
proprioceptive circuit and reconnect it to, for instance,
an escape circuit. Both mantids and tiger beetles
provide some support for the modular view: the components of the ultrasound-triggered evasive response in
flying mantids are very similar to those of the terrestrial deimatic (defensive) display (Yager and May, 1990);
the nocturnal response of flying tiger beetles to ultrasound—a fast, strong swing of the elytra into the
flapping hindwings—is the major component of the
landing response the same beetles use to evade robber
flies during the day (Yager and Spangler, 1997). Most of
the transformational mechanisms are likely to fall
somewhere between the extremes, especially for more
complex behaviors like mate attraction and courtship.
ACKNOWLEDGMENTS
My thanks to Jayne Yack, Martin Göpfert, Moira van
Staaden, and Annemarie Surlykke for very useful
discussions and for information on their newest insect
ear studies. Thanks also to Axel Michelsen who provided insightful comments that helped improve the
manuscript. This review was written with research
support provided by the University of Maryland, College Park.
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