Genetic Control of Acoustic Behavior in Crickets
RONALD R. HOY
Department of Nenrobiology and Behavior, Langmuir Laboratory,
Cornell University, Ithaca, New York 14850
SYNOPSIS. Evidence is presented that acoustic behavior in field crickets is under firm
genetic control. The calling song of adult males is highly stereotyped and species specific. Hybrids can be made by crossing two species of Teleogryltus with dissimilar calling
songs. The calling songs of the hybrids are uniquely different from that of either
parental species, and in addition the songs of the two reciprocal hybrids are different
from each other. Genetic control of song production is polygenic and multichromosomal; sex-linkage of some song determinants is also indicated. Female phonoresponse
to calling song was measured on a Y-maze. Species specificity of phonoresponse was confirmed and in addition, hybrid females prefer hybrid song to either parental song. The
possibility that calling song production in the male and its reception in the female are
genetically coupled is discussed.
INTRODUCTION
Field crickets (Family Gryllidae) and
other closely related insects such as grasshoppers, katydids, and cicadas produce
loud sounds ordinarily noticeable to man.
Acoustic behavior is very important in the
life of crickets. It meditates the reproductive and social interactions of the species.
On hot summer nights one is likely to hear
the calling sound of the male; only male
crickets sing. This long-distance song serves
the purpose of pair formation for reproduction: It attracts homospecific females into
a male's territory. Such behavior thus represents an intraspecific communication system in which the male cricket can be regarded as the "transmitter" of the signal
and the responding female the "receiver."
Once a male has attracted a female onto his
territory, he sings a courtship song which
Work on the genetic control of song production
was done at Dr. David Bentley's laboratory in the
Dept. of Zoology, University of California, Berkeley.
Studies on the phonoresponse of female crickets
were performed in the author's laboratory in the
Division of Biology, S.U.N.Y., Stony Brook, with
Mr. Robert Paul. Mr. John Paton, Section of Neurobiology and Behavior, Cornell University, provided
thoughtful suggestions regarding this manuscript.
I acknowledge support from the Public Health
Service-NIH during post-doctoral work with Dr.
Bentley, and for research grant NS 10176 CMS at
Stony Brook.
is different from the calling song and which
facilitates copulation; this song is apparently not species specific. If other males intrude upon his territory he might sing an
aggressive song. In this paper we shall be
concerned only with the calling song because its stereotypy and species specificity
lends itself to physiological and genetic
analysis.
The biological function of calling song
must be kept clearly in focus throughout
this review. It is the means by which a male
cricket communicates his species identity,
location, and reproductive readiness to potential mates. The song must therefore be
distinctive and stereotyped for the local
species as a whole and for any member in
particular. A female of the species must be
able to discriminate her conspecific song
from those of other singing insects in the
environment; her receptive apparatus must
be tuned to the calling song of her species.
It is precisely these biological constraints
which shape the calling song that have been
exploited in neurophysiological, behavioral,
and here, behavior genetic studies and that
make the cricket an attractive experimental
animal.
For extended discussions of acoustic behavior in crickets the reader is referred to
the excellent reviews of Alexander (1960,
1962, 1968).
1067
1068
RONALD R. H O Y
FIG. 1. Electromyograms recorded during the production of calling song in the hybrid T. oceanicus
9 X T. commodus $ (TJ. A, Oscillogram of sound
pulses (one phrase in the song is shown). B, Muscle
action potentials recorded from a wing opener, the
mesothoracic subalar. C, Muscle action potentials
from a wing closer, the mesothoracic promotor. Each
muscle potential was preceded by a single impulse
in the motor neuron that innervates the muscle
unit. Time calibration, 100 msec. (From Bentley and
Hoy, 1972.)
STEREOTYPY OF THE CALLING SONG
The variety of temporal patterns in calling
song depends on species; however, within
a given species the temporal structure is
rigidly stereotyped from male to male. It
is between species that pronounced song
differences can be observed. The song stereotypy within a given species serves as a
reliable standard against which genetically
based changes in song can be compared.
Coordinated behavior patterns are a
common theme of this symposium. The
calling song of field crickets is an excellent
example of a "fixed action pattern." The
temporal pattern of its components are
highly stereotyped and predictable within
a species. Many such behaviors have a central nervous system origin and are not dependent upon peripheral sensory cues to
generate the rhythm; several examples are
described in this symposium. The first demonstration of the central origin of rhythmic
behavior was that of Wilson (1961) for wing
movements during locust flight. Subsequently, several more behavior patterns
among the various invertebrates have been
shown to have a central origin (Willows et
al., 1973), including flight and calling song
in crickets (Bentley, 1969a,6).
Calling song is a procession of sound
pulses delivered in a predictable pattern.
A sound pulse is produced by a rapid closing stroke of the forewings, which bear specializations of the cuticle for sound production. The wings are reset by opening of the
forewings (during which no sound is produced). Thus, sound production is basically
a cyclic (open and close) activity in which
sound is produced by a frictional mechanism during the closing stroke. The timing
of contraction of opener and closer muscles
is precisely controlled by rhythmically alternating discharge of opener and closer
pools (Fig. 1). The motor system is thus
neurogenically controlled (Bentley and
Kutsch, 1966; Kutsch, 1969; Bentley, 19696).
INHERENT BASIS OF THE STEREOTYPY
OF CALLING SONG
It is not likely that crickets transmit their
song culturally, as is the case in higher
vertebrates and birds (Alexander, 1962;
Marler and Tamura, 1964). In temperate
regions with harsh winters crickets have but
a single generation per year; there is no
overlap of generations. Males can be raised
in individual isolation in the laboratory
and the calling songs are typical of the
species. Such observations point to the inherent nature of calling song.
Further evidence comes from the study
of the postembryonic development of song
patterns in nymphal crickets (Bentley and
Hoy, 1970). Crickets are hemimetabolous
insects that develop into an adult through
a series of nymphal stages. In Teleogryllus,
there may be from 9 to 11 molts before the
animal attains the sexually mature adult
form. Acoustic behavior is produced only
by adult males because it is not until the
final molt that fully developed wings (with
cuticular specializations for sound) appear.
We never observed Teleogryllus nymphs
moving their minute wing pads (wing pre-
GENETIC CONTROL OF ACOUSTIC BEHAVIOR IN CRICKETS
1069
C—jr-—f^i-Y^-W^W^nf^
•
i
FIG. 2. Electromyograms from a brain-lesioned, lastinstar nymph of Teleogryllus commodus. A, Electromyogram recorded from a wing opener muscle
(second basalar of the mesothorax). B, Oscillogram
of the calling song of T. commodus adult male. C,
Push-pull recording of myograms from antagonistic
muscles of the mesothorax: downward spikes are
from a wing opener (second subalar) and upward
spikes are from a wing closer (mesothoracic re-
motor). Note reciprocity of subalar-remotor firing
cycles in the nymph; this pattern is typical of adult
myograms during song production. The arrows in
trace A mark the switch from long intervals to short
intervals that is typical of the song as well as the
myograms of mature calling song. (From Bentley and
Hoy, 1970: copyright 1970 by the American Association for the Advancement of Science.)
cursors) with scissoring movements typical
of adult stridulatory movements. Thus,
nymphal crickets do not seem to perform
movements appropriate to acoustic behavior. Although the wings themselves are
not developed until adulthood, it is known
that most of the motor system underlying
flight including motor neurons and musculature are present from hatching (see Bentley, 1973, for a review of postembryonic
development). Huber (1962) discovered
that making lesions in the brain of adult
male crickets sometimes released spontaneous bouts of calling song. Adopting this
technique, Bentley and Hoy (1970) made
heat lesions in the mushroom bodies of the
brain of last instar nymphs of Teleogryllus
commodus. In a few cases this resulted in
spontaneous wing pad movements resembling adult stridulation. From wire electrodes inserted into the stridulatory
muscles, electromyograms resembling those
from stridulating adult males, even in important details of the output rhythm (Fig.
2), were recorded. Specifically, the motor
output of the nymph matches almost precisely that of an adult male producing the
species calling song, except that no sound
is produced during movements of the
nymph's wing pads. Thus, while normally
not active in the final instar nymph, the
neural circuitry underlying stridulation is
already established but apparently suppressed. Attempts to release song-like move-
ments from even earlier nymphal stages
were not successful.
From observations of life history, ontogeny, and neurophysiology, it is clear that
the characteristic rhythmic structure of
calling song-like movements is centrally
generated and shows little behavioral plasticity. It is to be expected that this behavior
is under firm genetic control.
GENETC CONTROL OF SONG PRODUCTION
Calling song is a highly stereotyped behavior which is easily quantified, and in
which even slight deviations from the typical species song can be easily detected. This
is an ideal situation for genetic analysis.
Our genetic studies (Bentley and Hoy,
1972) have involved several different species
in two genera of crickets. This paper will
be concerned with only two species of an
Australian field cricket, Teleogryllus
oceanicus and T. commodus. The calling
songs of these species are complex in that
they involve two pulse types, and the temporal relationships between pulses can be
classified into numerous stereotyped interpulse classes (Fig. 3, Table 1); this provides
ample material for genetic analysis. In a
previous genetic study (Leroy, 1966) it was
demonstrated that Fl hybrids could be
formed by crossing T commodus and T.
oceanicus. We produced F1 hybrids from
the reciprocal crosses:
1070
RONALD R. H O Y
Phrase
FIG. 3. Diagram of sound pulses in a phrase of the
calling song of Telegryllus. Upper, Calling song of
T. oceanicus. Lower, Calling song of T. commodus.
A song phrase is composed of two pulse types, louder
A-pulses and softer B-pulses. Interval structure can
be defined in terms of the diagram; intrapulse inter-
val: interval between successive A-pulses; intratrill
interval between successive B-pulses; and intertrill
interval: interval between last B-pulse in one trill
to the first B-pulse in the succeeding trill. (From
Bentley and Hoy, 1972.)
T-l: T. oceanicus $ X T. commodus o*
T-2: T. commodus } X T . oceanicus $
Many measurements of interpulse intervals
in parental and hybrid calling songs were
made. I shall simply summarize the results
of the crosses, which have been published
earlier (Bentley and Hoy, 1972).
Acoustic measurements were made from
parental and hybrid stocks by isolating
freshly molted, newly adult males individually and making tape recordings of their
calling song. Five males of each parental
type and ten of each hybrid type were tape
recorded during several minutes of steady
calling. Recording temperature was 24.5 ±
1 C. Interval measurements were made
from oscillograms obtained by filming the
oscilloscope display of the calling song from
the tape recorder. A typical section of film
contained 400 to 600 sound pulses. The
principal measurement was the interpulse
interval, which was defined as the interval
(in millimeters, which was later converted
to time) from the beginning of one pulse
and extending to the beginning of the next
one. From such data we produced interpulse interval histograms. This provided us
with a measure of the number, duration,
and variability of each interval class, as well
as displaying the different categories of intervals that make up the rhythmic structure
of the call.
A diagram of a single phrase of the calling songs in Teleogryllus would show that
oceanicus and commodus are easily distinguishable (Fig. 3). In both species a
phrase contains a "chirp" and "trill" portions. The trill in T. oceanicus is composed
of a series of doublet pulses, whereas they
are more continuous in T. commodus. A
diagram of a single phrase of the calling
songs of T. oceanicus and T. commodus
along with the terminology used to describe
them is shown in Figure 3.
A vigorously calling male sings 25 to 50
phrases per minute for many minutes. Each
phrase contains louder sound pulses (in the
"chirp" portion of the phrase) and softer
pulses (in the "trill"). Louder pulses are
produced by stronger excitation of the
motor system (Bentley and Kutsch, 1966;
Bentley and Hoy, 1972). The temporal pattern within a phrase is highly regular. It is
possible to measure the constancy of interpulse intervals within a chirp (intra-chirp
interval), within a trill (intra-trill interval),
between trills (inter-trill interval), and the
interval between successive phrases, the
phrase repetition rate (Table 1). It can be
seen from Table 1 that each species song
can be identified by characteristic values for
each interval type.
Since both parental species possess distinctly different song rhythms, the songs of
GENETIC CONTROL OF ACOUSTIC BEHAVIOR IN CRICKETS
1071
TABLE 1. Parameters of rhythm in Teleogryllus.
Parameter
Intra-chirp interval
Intra-trill interval
Inter-trill interval
No. of A-pulses per chirp
No. of B-pulses per trill
No. of B-pulses per phrase
No. of trills per phrase
Phrase repetition rate
Genotype
O
o/c
c/o
c
o
O/C
c/o
c
o
o/c
c/o
c
o
o/c
c/o
c
o
o/c
c/o
c
o
o/c
c/o
c
o
o/c
c/o
c
o
o/c
c/o
c
Mean
66.8
57.5
60.4
52.1
41.0
33.U
36.7
31.7
122.8**
136.9
154.0
160.9
4.8
4.2
4.9
5.9
2.0*
4.5
4.9
10.7
20.9
18.4
19.4
21.5
9.4*
4.2
4.8
2.3
28.5
37.5
33.0
41.7
Standard
deviation
6.7
6.5
6.1
6.8
1.3
3.8
5.0
3.5
14.1"
23.6
38.8
60.6
0.9
0.6
0.7
0.9
0.1*
1.5
2.0
5.3
3.0*
4.9
4.7
10.4
2.3
1.0
1.2
1.2
2.4* •
5.3
7.0
18.1
n
290
712
807
489
740
2833
2450
1840
813
837
693
119
100
100
, 100
100
250
194
200
147
38
28
37
34
100
100"
100
100
77
105
70
102
O = X. oceanicus (5 individuals); O/C=T. oceanicus $ X T. commodus $ (10 individuals); C/O=7".
commodus $> X T. oceanicus Jj (10 individuals); C = T. commodus (5 individuals). Intervals in milliseconds, repetition rate in phrases per minute.
•Hybrids significantly different from both parental types.
"Hybrids significantly different from each other and from both parental types. (From Bentley and Hoy,
1972.)
Fx hybrid males will reflect genetic differences (Fig. 4). Qualitatively we see that the
doublet pulse in the trill of T. oceanicus is
not present in the F^ Quantitatively, most
of the parameters we used to characterize
the song rhythm of the F/s were intermediate between the parental values (Table 1).
Examples include intratrill and intrachirp
intervals. We found no Fx interval measurements that fell within either parental range,
thus making unlikely a simple dominancerecessive genetic control of song. Intermediate inheritance usually indicates polygenic
control or possibly monofactorial inheritance with incomplete penetrance. Exami-
nation of backcross hybrids distinguishes
between these two possibilities, and in the
case of Teleogryllus polygenic inheritance
is indicated (Bentley, 1971). This confirms
the earlier conclusion of Leroy (1966) that
polygenic inheritance occurs in Teleogryllus songs.
Certainly, the hybrid calls are different
from either parental call. Moreover, further
analysis revealed that the two reciprocal
hybrids (T t and T2) were different from
each other specifically in the duration and
variability of the inter-trill interval, and in
phrase repetition rate (Fig. 5; Table 1).
Traits that differ between reciprocal hy-
1072
RONALD R. HOY
FIG. 4. Oscillograms of the calling song of Teleogryllus and its F; hybrids. A, T. oceanicus B, T.
oceanicus 9 X T. commodus $ (T,); C, T. commodus J X T. Oceanicus $ (T2); D, T. commodus.
Arrows indicate the end of one phrase and the be-
ginning of the next one in the calling song. The hybrids T, and T™ have calling songs with a different
rhythmic structure than either parental song. Time
calibration, 0.5 sec. (From Bentley and Hoy, 1972.)
brids are likely due to sex-linked factors.
Crickets have XO sex determination since
crickets lack the Y-chromosome. Thus,
males get their single X-chromosome from
their mother. Sex-linkage of song traits implies that such traits would be more characteristic of the song of the maternal species
than of the paternal species. In the case of
inter-trill interval and phrase repetition
rate this is precisely the situation (Table
1). Hybrid T j (T. oceanicus 9 /T. commodus cf), which gets its X-chromosome
from T. oceanicus, sings a calling song with
a well-defined inter-trill interval (see arrow
in Fig. 5) that is present in the call of its
maternal species, T. oceanicus. The intertrill interval is lacking in the reciprocal
hybrid T 2 which gets its X-chromosome
from T. commodus, whose call lacks a discretely defined inter-trill interval. Thus,
some factors determining temporal pattern-
ing in calling song reside on the X-chromosome.
The genetic control of song production
can be summarized as follows:
1) Most of the parameters of song
rhythm, such as the intra-chirp and intratrill intervals are intermediate in the F,
compared to parental values, and are similar between both reciprocal hybrids. This
indicates polygenic inheritance of song distributed among the autosomes. Hybrids Tx
and T 2 are different from either parent in
song type.
2) A few parameters of rhythm, such as
inter-trill interval and phrase repetition
rate are strongly affected by sex-linked factors. Hybrid Tj differs from T 2 in song
type.
3) Since temporal pattern of calling song
is controlled through factors residing on an
unknown number of autosomes as well as
1073
GENETIC CONTROL OF ACOUSTIC BEHAVIOR IN CRICKETS
T. commodus
N»500
C?xO/hybrtd
N-370
40
80
120
160
200
Inter
FIG. 5. Interpulse interval histograms of the calling
songs of TeleogryUus and its F, hybrids. Each histogram constructed from a portion of calling song of
one individual. The number of pulses in the portion
of song analyzed is given by "X." Such histograms
were made for many individuals and ones above are
representative of each species or hybrid type. Each
0
40
80
pulse Interval (m»)
120
160
200
249
histogram can be divided into three modes which
are, from left to right, intratrill interval, intrachirp
interval, and intertrill interval. Intervals are measured in milliseconds. The arrow indicates sexlinked control of the intertrill interval (see text).
(From Bentley and Hoy, 1972.)
1074
RONALD R. HOY
the X-chromosome, genetic control is exerted multichromosomally as well as polygenically.
GENETIC CONTROL OF SONG DISCRIMINATION
In the beginning of this review I stressed
the point that acoustic behavior in crickets
is to be regarded as a communication system. In the section just concluded the
genetic control of the transmitter of the
cricket communication system was described. I now turn to the effects of shuffling
genotypes around in the receiver, e.g., what
is the response of hybrid females to the
calling song of her parental species, or of
her male sibling? I will again summarize
previous studies (Hoy and Paul, 1973).
Phonotaxis is locomotion directed toward
a sound source and is readily demonstrated
in female crickets (Regen, 1913; Walker,
1957; Murphey and Zaretsky, 1972). We
chose to test the relative "attractiveness" of
parental and hybrid cricket songs for a
female cricket by placing tethered females
on a Y-maze, and placing the entire apparatus in a directional sound field (Fig. 6).
This procedure is an adaptation of the
Y-maze technique employed in studies of
the optomotor reaction of insects in which
the steering input was visual rather than
acoustic (Reichardt, 1961; Wilson and Hoy,
1968). The tethered female accepts the
styrofoam maze as a substrate and suspends
it in mid-air. The maze consists of three
straight paths, 10.5 mm in length, interconnected by two Y choice points. Thus, a
walking female is actually moving the maze
beneath her; at each point she must choose
either the left or right arm of the maze,
putting her back on a straight path followed
by another Y-junction, etc. By playing calls
through a loudspeaker on the cricket's right
or her left, we measured the relative attractiveness of a particular song by counting
how many times she chose the arm of the
maze that corresponds to the direction of
the sound. It is important to note that the
cricket does not actually change her orientation to the sound; the loudspeaker is always at a fixed angle to the animal. The
only things that move in our set-up are the
FIG. 6. Drawing of a female cricket tethered to
supporting apparatus above her. She is holding a
styrofoam Y-ma/.c, which is suspended in mid-air.
Calling songs are played from loudspeakers that are
symmetrically placed on her left and right.
animal's legs (propelling the maze backwards) and the maze itself. We played loudspeakers at an angle of 40° from the
cricket's longitudinal axis and facing the
animal, symmetrically on her right and left.
We required each female to make 40
choices, 20. when the sound played from the
right (or left) speaker and 20 when the
sound was played from the opposite
speaker. The ratio of choices toward the
sound source to total number of choices (20
in each direction) was taken as an index of
the relative attractiveness of the song. This
value was defined as the phonomotor response, r, in analogy with the optomotor
experimental terminology (Reichardt, 1961;
Hoy and Paul, 1973). Thus, we can determine for each female, r values for the songs
coming from her right and from her left.
It should be obvious that r varies between
0 and 1.0; if no choices were made toward
the sound source, r = 0, if all choices were
made toward the sound source, r — 1.0, and
if only half of the turns were toward the
sound, r = 0.5. Tape loops of the calling
songs of T. commodus, T. oceanicus, and
the hybrid T1 (T. oceanicus 9 X T. commodus cf) were presented to tethered
GENETIC CONTROL OF ACOUSTIC BEHAVIOR IN CRICKETS
females on the Y-maze. We matched the
temperature at which a calling song was
recorded to the temperature during each
maze experiment, within 2 C. Intensity of
the calls measured at the maze was 69 db
relative to 2 x 10~4 ^bar.
The performances of 147 adult, virgin
female crickets in Y-maze experiments were
analyzed (Fig. 7). We displayed r values
for right and left sound directions in the
form of a scattergram. Each point represents the performance of a single individual
female for 20 choices with respect to each
sound direction; her performance with respect to sound from her right can be determined by reading across the scattergram,
and her performance to sound from her left
is seen by reading down the scattergram.
The results show a tendency for clustering
of points when the song played matches the
species of the cricket on the maze, i.e., r
values tend to approach 1.0 for both directions of sound (Fig. 7). When the song does
not match the species of the cricket on the
maze, r values tend to be more dispersed.
We interpret this to mean that female
crickets are attracted more to the calling
song of their own species than to a different
species. This result is precisely what would
be expected in nature (Alexander, 1968)
and has been demonstrated for free-walking
animals in our own laboratory and others
(Walker, 1957; Hill et al., 1972). It is important for our purposes because it validates the Y-maze technique for measuring
phonotaxis; there was no a priori assurance
that the maze technique would work. The
surprising result was the performance of
hybrid females on the maze. By the criteria
established above it appears that the hybrid
females prefer the calling songs of their
brothers, more than either parental species
calling song.
The results are made clearer by the following procedure. We arbitrarily define a
phonomotor response to be a strong one if
it meets the criterion of having r values of
0.75 or greater (at least 15 of 20 turns
directed toward the sound) for both sound
directions. We then tally the number of
females that meet this criterion and compare it with the total number of females
1075
in the test (Table 2). Thus, we see that with
T. oceanicus on the maze, 14 out of 22
females met the criterion when they were
played the calling song of T. oceanicus, but
only 4 met the criterion when played the
heterospecific calling song of T. commodus.
As suggested by visual inspection of the
scattergram (Fig. 7), T. oceanicus prefers
homospecific song to heterospecific song.
The results in Table 2 are significant at the
1% confidence level (G-test of independence).
To summarize, we find that the results of
phonotaxis experiments are confirmed in
the phonomotor test: females are attracted
to homospecific song more than to heterospecific song. In addition, hybrid females
find the calling song of their male siblings
more attractive than either parental calling
song.
The performance of some females during
maze tests requires further comment (Fig.
7, arrow). Some female crickets tended to
choose one direction almost exclusively, no
matter what the direction of sound. This
behavior was more likely to occur when the
cricket was played heterospecific song. This
is seen by the increased scatter of points
during tests of heterospecific song (Fig. 7)
and the failure to meet the criterion for
strong phonomotor response (Table 2). It
is likely that such animals were showing
locomotory preference toward either the
right or the left in the absence of steering
input; thus, an animal will circle constantly
to the right (or left) in the dark (Wilson
and Hoy, 1968). Crickets will not walk on
the maze unless stimulated by calling song.
We find that when the speaker is placed
directly in front of the cricket, rather than
off to its right or left, it will walk, but with
a locomotory bias toward one side or the
other. We tested animals, such as the one
indicated by the arrow in Figure 1 which
performed on the maze as though they were
indifferent to the direction of the sound
source, for locomotory bias. When played
calling song from a speaker directly in front
of them, they tended to show phonomotor
behavior identical to that produced when
the speakers were placed directionally.
Thus, at least part of the scatter that occurs
1076
RONALD R. H O Y
T. commodus
T. commodus
I.On
J> d>°
T. oceanicus
o
o
qpo
o
o
o
o _
§ 0.5-
1
I
1
T. oceanicus
1.0
Left
I
0
I
1
0.5
1.0
T. oceanicus
T. commodus
L0-|
o
o
o
&
o
o
o
tf>
°<Po
O 0
<$»
S?
o o
o
o
o
oo
o
o
oo
1
°S
I
OO
O
1.0
l
0.5
0
Left
T. oceanicus
o
. _ T. commodus
O
1
1 —)
0.5
T-l Oc^/Co
1.0—|
T
7
0.5
O
I
\.o
00
o
o
o
o
o
|0.5H
i
0.5
r
10
6
o!s
1.0
i
i
0.5
r
1.0
Left
FIG. 7. Scattergrams displaying the phonomotor
response of Teleogryllus and hybrid F, females in
response to homospecific and heterospecific calling
songs. The horizontal and vertical axis of each
scattergram records the phonomotor response ratio
when song was played from left and right speakers
respectively. Each point represents the performance
of a different female. The top pair of scattergrams
represents the performance of T. commodus females
on the Y-maze when played T. commodus calling
song (left scattergram) and T. oceanicus song (right
scattergram). Similarly the middle pair of scattergrams illustrates the performance of T. oceanicus
females to homospecific and heterospecific calling
song. The bottom trio of scattergrams represents
the performance of the hybrid T^ females, (T.
oceanicus 9 X 7 " . commodus $) when played the
calling songs of T. commodus, T. oceanicus, and
that of sibling T-l males. (From Hoy and Paul,
1973: copyright 1973 by the American Association
for the Advancement of Science.)
GENETIC CONTROL OF ACOUSTIC BEHAVIOR IN CRICKETS
TABLE 2. Comparison of phonometer response of
147 female crickets to conspecific and heterospecific
calling songs. (From Hoy and Paul, 1973.)
Calling song
T. oceanicus
T. commodus
T. oceanicus
T. commodus
T. oceanicus
T. commodus
Hybrid (T,)
Females at
criterion/
total
tested
T. oceanicus on maze
14/22
4/22
T. commodus on maze
3/15
21/28
Hybrid (T,) on maze
3/11
8/21
21/28
Females
at
criterion
(%)
63.6
18
20
75
27.3
38
75
in Figure 7 might be attributable to locomotory bias. Why an animal is more likely
to show locomotory bias when played
heterospecific song than when her homospecific song is played is unknown; we interpret it to be an indication of discriminatory behavior by the animal.
THE GENETIC CONTROL OF A COMMUNICATION
SYSTEM
Hybrid male crickets of Teleogryllus
produce calling songs that are distinctly
different from either parental song and
these differences can be attributable to
genetic factors. Hybrid females apparently
find the calling song of sibling males more
attractive than the song of either parental
species. Presumably, this, too, has a genetic
basis. Taken at face value these results indicate that whatever the precise nature of
the genetic control, both the male (signal
transmitter) and the female (signal receiver)
are "coupled together" with respect to their
acoustic communication system. That is, the
receptive apparatus of the hybrid female is
somehow tuned to the song of the hybrid
male. While this is clearly an appealing
way to design a communication system, this
interpretation requires caution. For example, we have shown that most of the
temporal parameters of the calling song in
the hybrid male are intermediate between
those of its parental species. Perhaps it is
simply the case that the receptive apparatus
1077
also becomes intermediate in its sensitivities
to various aspects of the call. Besides
rhythm, what other aspects of the song
might be important? We have not mentioned the carrier frequency in Teleogryllus
song. In T. commodus it is about 3.5 kHz
and in T. oceanicus it is about 4.5 to 5 hKz
(Leroy, 1964; Hill et a!., 1972; unpublished
measurements in our own laboratory). The
carrier frequency of hybrid calls is often
intermediate (Leroy, 1964), but there is considerable variation among sibling hybrids,
based on measurements taken of our specimens. It is generally conceded that the
species-specificity of calling song resides in
the temporal pattern of the call (Alexander, 1968; Zaretsky, 1972) but it is possible that carrier frequency plays some role
(Loftus-Hills et al., 1971). We have proceded on the assumption that rhythm is the
most crucial component for communication. While most of the parameters of
rhythm in the hybrid call are intermediate,
we found that the inter-trill interval and
the phrase repetition rate are affected by
sex-linkage and serve to differentiate the
calls of the two reciprocal hybrids, i.e., the
call of hybrid T1 (oceanicus $ /commodus
cf) is different from that of hybrid T 2
(commodus $ /oceanicus o*). It is therefore
crucial to measure the phonoresponse of
T x and T 2 hybrid females in response to
T x and T 2 calls. If Tx females can discriminate T x calls from T 2 calls, and vice-versa,
then the simple hypothesis that the matching of hybrid male's song with hybrid female's sensitivity is due to inheritance of
an intermediate state in each system, is
unlikely. Parameters of rhythm that are
intermediate in the hybrid call, such as
intra-trill and intra-chirp interval, do not
differentiate T x from T 2 calls, and hence
cannot provide cues for T x and T 2 females
to perform a discrimination. Thus, discrimination tests of the reciprocal hybrid females
T x and T 2 in response to the calling songs
of both reciprocal males are critical to further interpretation on the genetic control
of acoustic behavior. These experiments are
in progress in our laboratory.
While considerable information is available about the neural basis underlying song
1078
RONALD R. HOY
production and its genetic control (Bentley
and Kutsch, 1966; Bentley, 19696, 1971;
Kutsch, 1969; Bentley and Hoy, 1972), not
much is known about the neural processing
of acoustic signals in the cricket, let alone
its genetic basis. Recent studies (Popov,
1971; Nocke, 1972; Stout and Hubner, 1972;
Zaretsky, 1972) have provided new insights
about sensory coding of acoustic signals,
such as pattern sensitivity in auditory interneurons, but knowledge still lags that in the
motor system. It is fashionable to speak of
"pattern generators" in the motor systems
of invertebrates (see other papers in this
symposium) and the notion that there exists
"sensory filters" or "feature detectors" in
sensory systems (both vision and audition)
has been proposed (Lettvin et al., 1959;
Frishkopf et al., 1968; Capranica, 1969). It
is obvious from other papers in this symposium that "pattern generator" in motor
systems can be defined in fairly explicit
anatomical and neurophysiological detail.
As yet, it is not possible to say whether the
notion of sensory filters is embodied in a
property of single neurons or of a network
of neurons. The interpretation of our genetic results at the level of the nervous
system is obviously premature. Nonetheless
behavioral results suggest that it is useful to
think in terms of species-specific song templates, such as have been suggested for birdsong (Konishi, 1963). If Teleogryllus
females have com modus and occanicus species templates, then a genetic cross would
result in hybrid templates. Since females
cannot announce their identities as do calling males, their genetic identity is revealed
by song discrimination in phonomotor behavior.
This brings us back to the possible
genetic coupling of acoustic communication
in crickets. Our results imply that the behavioral coupling has its basis in genetic
coupling of the pattern generator in the
male and song template in the female. How
can a set of genes control properties of
neurons concerned with motor output in
males and neurons concerned with auditory
input in females such that both are commonly attuned to each other? For reasons
mentioned above, it is pointless to carry
speculation any farther. However, whatever
the mechanism, it must be stressed that such
a coupling has profound evolutionary implications because it would provide a
possible mechanism for speciation by hybridization. Evolutionary biologists have
long recognized the attractiveness of coupling together transmitter and receiver in
a communication system (Alexander, 1962).
The coupling of song transmission and
song reception by a common mechanism(s)
receives indirect support from another behavioral study. It is a matter of folklore
that a cricket's chirp rate depends on ambient temperature, slower at low temperatures and faster at high temperatures. In
modern times this observation has been
quantitatively measured for several cricket
species (Walker, 1962). Walker (1957) also
reports the phonotaxic behavior of the female to her conspecific (or electronically
simulated) calling song appears to be temperature sensitive. Specifically, Walker
found that "the specific pulse rate to which
the female exhibits greatest response varies
with temperature in the same manner as
does the pulse rate in the song of the male"
(Walker, 1957, p. 636). No speculations
about the central nervous origin of the
temperature-sensitive acoustic mechanisms
were made in this study. I simply point out
that this observation is consistent with the
notion that the male song pattern generator
and the female sensory template (which
might or might not have a common element) are coupled together, both behaviorally and genetically. Again, speculating on
the CNS origin is premature at this time.
RELATION OF THESE STUDIES TO BEHAVIOR
GENETICS
We have seen in this symposium two different approaches to behavior genetics. One
is the analysis of the effects of single gene
mutations on behavior. This is greatly
facilitated by the ability to generate mutants by means of chemical agents or by
irradiation. This strategy has been spectacularly successful in invertebrates like Dorsophila (Hotta and Benzer, 1969; Benzer,
1971; Suzuki et al., 1971; Ikeda, 1974) as
GENETIC CONTROL OF ACOUSTIC BEHAVIOR IN CRICKETS
well as to vertebrates like mice (Sidman,
1968). While such studies are of great importance for producing fine resolution genetic maps of behavioral foci, and will
undoubtedly forge the link between development and genetics in studies of the
structure and function of the nervous system, they have certain shortcomings. The
mutations usually have lethal or at least
debilitating effects upon the animal; behavior is affected through major regulative
neural functions. This limitation is due to
restrictions imposed by methods of detecting (screening) behavioral mutants. While
these studies are of fundamental value in
neurogenetics it is not likely that natural
populations become behaviorally differentiated by gross mutational changes of this
type.
If one's primary interest is in the evolution of behavioral systems, then one is
forced to examine deviations in normal
behavior of a less drastic type. Unfortunately, complex behavior is usually under
polygenic control (Ewing and Manning,
1967). The distribution of genetic control
over a number of different genes can be
rationalized in terms of buffering the system against serious alteration by chance
mutations in a single gene. Whatever the
benefit for the animal, it makes doing behavior genetics a more difficult task. Moreover, the problem is complicated by the
inability to "quantize" behavior into discrete units; the occurrence or nonoccurrence
of behavior is often a matter of "thresholds"
(Ewing and Manning, 1967).
At this point it is appropriate to mention
a few advantages for studying behavior
genetics in the cricket. As described in the
present paper and elsewhere (Bentley and
Kutsch, 1966; Bentley, 19696, 1971; Bentley
and Hoy, 1972) the stereotypy of the calling
song provides "units" for physiological, behavioral, and genetic manipulation. The
fact that acoustic behavior is the communication system responsible for preserving the
species provides an opportunity to relate
behavior genetics to the evolution of behavior. Thus, genetic analysis moves beyond
a neurological subsystem in a single individual because acoustic behavior is presum-
1079
ably a coupled system in which the sender
and receiver must always be in step, at the
great risk of not adding one's genes to
future generations. In mate attraction
crickets must be very conservative; it is
nowhere more true than for crickets: "different strokes for different folks."
There are, of course, limitations for using
the cricket in behavior genetics. Not the
least is the fact that we know almost nothing about its genetic mapping, which would
be a formidable undertaking when one
notes that Teleogrylhis contains 29 pairs of
chromosomes (Leroy, 1967). However, it is
possible to induce allele mutations in
crickets (Bentley, personal communication)
and hence in principle, to make chromosomal maps.
Our studies in the cricket are complementary to those in Drosophila and both
reaffirm the choice of invertebrate animals
as appropriate subjects for the study of behavioral and neurogenetics.
REFERENCES
Alexander, R. D. 1960. Sound communication in
Orthoptcra and Cicadidae, p. 38-92. In W. E.
I.anyon and W. X. Tavolga (ed.), Animal sounds
and communication. Amer. Inst. of Biol. Sci.,
Washington, D.C.
Alexander, R. D. 1962. Evolutionary change in
cricket acoustical communication. Evolution 16:
443-467.
Alexander, R.D. 1968. Arthiopods, p. 167-216. In
T. Sebeok (cd.), Animal communication. Indiana
Univ. Press, Bloomington.
Bentley, D. R. 1969n. Intracellular activity in cricket
neurons during generation of song patterns. Z.
Vcrgl. Physiol. 62:267-283.
Bentley, D. R. 19696. Intracellular activity in cricket
neurons during generation of behavior patterns.
J. Insect Physiol. 15:677-700.
Bentley, D. R. 1971. Genetic control of an insect
neuronal network. Science 174:1139-1141.
Bentley, D. R. 1973. Postembryonic development of
insect motor systems, p. 147-178. In D. Young
(ed.). Development neurobiology of Arthropods.
Cambridge Univ. Press, Cambridge.
Bentley, D. R., and R. R. Hoy. 1970. Postembryonic
development of adult motor patterns in crickets:
a neural analysis. Science 170:1409-1411.
Bentley, D. R., and R. R. Hoy. 1972. Genetic control of the neuronal network generating cricket
song patterns. Anim. Behav. 20:478-492.
Bentley, D. R., and W. Kutsch. 1966. The neuromuscular mechanism of stridulation in crickets.
J. Exp. Biol. 45:151-164.
1080
RONALD R. HOY
Benzer, S. 1971. From the gene to behavior. J. Amer.
Med. Ass. 218:1015-1022.
Capranica, R. R. 1969. A model system: vocalization
in frogs. Neurosci. Res. Program Bull. 7:427-436.
Ewing, A. W., and A. Manning. 1967. The evolution
and genetics of insect behavior. Ann. Rev. Entomol. 12:471-494.
Frishkopf, L. S., R. R. Capranica, and M. H. Goldstein. 1968. Neural coding in the bullfrog's auditory system: a teleological approach. I.E.E.E. Proc.
56:969-980.
Fuller, J. L., and W. R. Thomson. 1960. Behavior
genetics. John Wiley and Sons, N.Y.
Hill, K. G., J. J. Loftus-Hills, and D. F. Gartsidc.
1972. Pre-mating isolation between the Australian
field crickets Teleogryllus commodus and T.
oceanicus. Aust. J. Zool. 20:153-163.
Hotta, Y., and S. Benzer. 1969. Abnormal electroretinograms in visual mutants of Drosophila.
Nature (London) 222:354-356.
Hoy, R. R., and R. C. Paul. 1973. Genetic control
of song specificity in crickets. Sci. 180:82-83.
Huber, F. 1962. Central nervous control of sound
production in crickets and some speculations on its
evolution. Evolution 16:429-442.
Ikeda, K., and \V. D. Kaplan. 1974. Neurophysiological genetics in Drosophila melanogaster.
Amer. Zool. 14:
Konishi, M. 1963. The role of auditory feedback in
the vocal behavior of the domestic fowl. Z.
Tierpsychol. 20:349-367.
Kutsch, W. 1969. Neuromuskulare Aktivitat bei
verschiedenen Verhaltensweisen von drei Grillenarten. Z. Vergl. Physiol. 63:335-378.
Leroy, Y. 1964. Transmission du parametre frequence
dans Ie signal acoustique des hybrides Fl et PxFl,
de deux Grillions: Teleogryllus commodus Walker
et T. oceanicus. C. R. Acad. Sci. Paris 259:892-895.
Leroy, Y. 1966. Signaux acoustiques, comportement
et systematique de quclque especes de Gryllidcs
(Orthopteres, Ensiferes). Bull. Biol. Fr. Belg. 100:
63-134.
Leroy, Y. 1967. Garnitures chromosomiques ct
systematique des Grillinae (Insectes Orthopteres).
C. R. Hebd. Seances Acad. Sci. Paris 264:2307-2310.
Lettvin, J. Y., H. R. Maturana, W. S. McCulloch,
and W. H. Pitts. 1959. What the frog's eye tells
the frog's brain. Proc. Inst. Radio Engr. 47:19401951.
Loftus-Hills, J. J., M. J. Littlejohn, and K. G. Hill.
1971. Auditory sensitivity of the crickets Teleogryllus commodus and T. oceanicus. Nature (London) 223:184-185.
Marler, P., and M. Tamura. 1964. Culturally transmitted patterns of vocal behavior in sparrows.
Sci. 146:1483-1486.
Murphey, R. K., and M. D. Zaretsky. 1972. Orientation to calling song by female crickets, Scapsipedus
marginatus (Gryllidae). J. Exp. Biol. 56:335-351.
Xocke, H. 1972. Physiological aspects of sound communication in crickets (Gryllus campeslris L.) J.
Comp. Physiol. 80:141-162.
Popov, A. V. 1971. Synaptic transformation in the
auditory system of insects, p. 301-320. In G. V.
Gersuni (ed.), Sensory processes at the neuronal
and behavioral levels. Acad. Press, N.Y.
Regen, J. 1913. Ober die Anlockung des Weibchens
von Gryllus campestris L. durch telephonisch
libertragene Stridulationslaute des Mannchens.
Pfluger's Arch. Gesamtc Physiol. 155:193-200.
Reichardt, W. 1961. Autocorrelation, a principle for
the evaluation of sensory information by the central nervous system, p. 303-319. In W. A. Rosenblith (ed.), Sensory communication. M.I.T. Press,
Cambridge, Mass.
Sidman, R. 1968. Development of interneuronal
connections in brains of mutant mice, p. 163-193.
In F. D. Carlson (ed.), Physiological and biochemical aspects of nervous integration. Prentice-Hall,
Inc., New Jersey.
Stout, J. F., and F. Huber. 1972. Response of central
auditory neurons of female crickets (Gryllus campestris L.) to the calling song of the male. Z.
Vergl. Physiol. 76:302-313.
Suzuki, D. T., T. Grigliatti, and R. Williamson.
1971. Temperature-sensitive mutations in Drosophila melanogaster, VII. A mutation causing reversible adult paralysis. Proc Nat. Acad. Sci. U.S.A.
68:890-893.
Walker, T. J. 1957. Specificity in the response of
female tree crickets (Orthoptera, Gryllidae,
Oecanthinae) to calling songs of the males. Ann.
Entomol. Soc. Amer. 50:626-636.
Walker, T. J. 1962. Factors responsible for intraspecific variation in the calling songs of crickets.
Evolution 16:407-428.
Willows, A. O. D., D. A. Dorsett, and G. Hoyle.
1973. The neuronal basis of behavior in Tritonia.
III. Xeuronal mechanisms of a fixed action pattern. J. Neurobiol. 4:255-285.
Wilson, D. M. 1961. The central nervous control of
flight in a locust. J. Exp. Biol. 38:471-490.
Wilson, D. M., and R. R. Hoy. 1968. Optomotor reaction, locomotory bias, and reactive inhibition in
the milkweed bug Oncopeltus and the beetle
Zophobas. Z. Vergl. Physiol. 58:136-152.
Zaretsky, M. D. 1972. Specificity of the calling song
and short term changes in the phonotactic response by female crickets Scapsipedus marginatus
(Gryllidae). J. Comp. Physiol. 79:153-172.