Download Convergent song preferences between female

Behavioral Ecology Vol. 7 No. 3: 279-285
Convergent song preferences between female
field crickets and acoustically orienting
parasitoid flies
William E. Wagner, Jr.
Nebraska Behavioral Biology Group, School of Biological Sciences, University of Nebraska-Lincoln,
Lincoln, NE 68588, USA
Traits that increase the attractiveness of males to females often make them more conspicuous to predators. In the field cricket
(Gryilus lineaticeps), males are attacked by parasitoid tachinid flies (Ormia ochracea) that locate males through their calls. Female
flies larviposit on crickets and the larvae burrow into and feed on the cricket, killing the cricket upon emergence. To determine
whether traits preferred by females increase a male's risk of attracting a predator, I examined the effect of variation in male
singing behavior on mate and predator attraction. Both female crickets and female flies preferred male calling songs with higher
chirp rates, longer chirp durations, and higher chirp amplitudes. In addition, both female crickets and female flies preferred
male calling songs with higher chirp rates and longer chirp durations, even when these songs were of lower amplitude. These
results suggest that sexual selection by female choice will favor the evolution of higher chirp rates and longer chirp durations.
However, call types that increase a male's attractiveness to females also appear to increase a male's risk of attracting parasitoids.
Sexual and natural selection appear to have opposing effects on the evolution of male singing behavior in this species. Key
words: female choice, field crickets, Gryilus lineaticeps, Ormia, parasitoid, predation, sexual selection, tachinid flies. [Behav Ecol
7:279-285 (1996)]
I
n many animals males possess conspicuous structures or
produce elaborate displays that function, in part, to attract
females for mating (reviewed by Darwin, 1871; Kirkpatrick,
1987b; Searcy and Andersson, 1986; Thornhill and Alcock,
1983). Females often select mates based on variation in male
morphology or behavior, resulting in sexual selection on these
traits (Endler, 1980; Price, 1984; Ryan, 1985; Sullivan, 1987).
Male traits preferred by females also can make a male more
conspicuous to predators (Endler, 1980; Ryan et al., 1982).
Sexual selection by female choice and natural selection by
predation may thus have opposing effects on the evolution of
male traits. In general, the state of male traits preferred by
females is thought to reflect a balance between natural and
sexual selection (Endler, 1982; Fisher, 1958).
In field crickets, males commonly sing from within or near
burrows to attract females (Alexander, 1961), and females often select mates based on variation in male calling song (Hedrick, 1986; Popov and Shuvalov, 1977; Simmons, 1988; Walker,
1957). The calling song of some species also attracts parasitoid
female tachinid flies of the genus Ormia (e.g., Cade, 1975;
Walker, 1986). These flies possess a unique hearing organ that
allows them to locate singing males (Robert et al., 1992), and
female flies discriminate between species of field cricket based
on male calling songs (Walker, 1986, 1993). Once a male
cricket is located, a female fly deposits larvae on and around
the cricket (Cade, 1975). The larvae burrow into the cricket,
feed, and grow. Approximately 7 days after entering a cricket
the larvae emerge and pupate, killing the host.
Fly predation may favor both the evolution of noncalling,
satellite mating tactics and reduced nightly singing duration
in male field crickets (Cade, 1975, 1979; Cade and Wyatt,
1984). In addition, fly predation may produce evolutionary
changes in male calling song structure (Zuk et al., 1993). It
Received 27 February 1995; revised 11 July 1995; final revision 25
August 1995; accepted 25 August 1995.
1045-2249/96/S5.00 © 1996 International Society for Behavioral Ecology
is not known, however, if, within a species, some types of calling songs are more likely to attract flies than others, although
studies have shown that interspecific variation in song structure can affect the attractiveness of songs to flies (Walker,
1993). Flies might discriminate between cricket song types for
at least two reasons. First, some types of song may be easier
for flies to localize. Second, songs may contain information
about host quality. Other parasitoids are known to discriminate between hosts based on host quality (reviewed by Godfray, 1994).
In this article I test the hypothesis that parasitoid flies are
preferentially attracted to the same types of calling songs as
females in the field cricket Gryilus lineaticeps. Male singing
behavior can vary in a number of ways, including the rate at
which chirps are produced, the duration of chirps, and the
rate at which pulses are produced within chirps (Wagner WE,
unpublished data; Weissman et al., 1980; Figure 1). While G.
lineaticeps has not previously been reported to be a host for
Ormia, larvae of O. ochracea have emerged from male crickets
that I collected in the field. First, I examined the influence
of male chirp rate and chirp duration on mate and fly attraction. Second, I examined the influence of chirp amplitude on
mate and fly attraction. Although chirp amplitude can potentially vary among males, the amplitude of a sound for the
receiver primarily depends on the distance of the receiver
from the animal producing the signal (e.g., Michelsen, 1985;
Piercy et al., 1977). Consequently, chirp amplitude likely provides information primarily about a male's distance. Third, I
examined the relative importance of chirp rate and chirp duration in mate and fly attraction. Fourth, I examined the amplitude dependence of mate and fly preferences based on
chirp rate and chirp duration. In some animals mating preferences can be eliminated by reducing the amplitude of the
preferred signal (e.g., Gerhardt, 1991), suggesting that these
animals either prefer signals that are more conspicuous or are
unwilling to travel longer distances to mate with a male producing a preferred signal type.
Behavioral Ecology Vol. 7 No. 3
280
Table 1
Stimuli used to test female cricket and By song preferences
Test Stimulus
1
2
3
300
4
Figure 1
Waveform of the calling song of a male field cricket, G. limaticeps.
METHODS
Preferences of female field crickets
Female choice based on variation in male calling song was
tested in the laboratory from 1 July to 11 July 1994. Females
used in the tests were offspring of field-caught crickets from
Tucker's Grove County Park, Santa Barbara, California. Crickets were raised in a common culture (a 45 1 plastic trash can)
provisioned with water, cat food, oviposition dishes containing
moist vermiculite, and cardboard egg cartons. Prior to their
final molt, females were removed from the culture and isolated in individual containers to ensure that all females tested
were virgins. Females were tested between 10 and 21 days after
their final molt Females are both sexually mature and receptive to mating at this time (Wagner WE, personal observation).
Female preferences were tested using six pairs of stimuli
(Table 1). The chirp rates and chirp durations used fall within
the natural range of variation for male calling song; chirp
rates vary between 0.83 and 4.65 chirps/s, while chirp durations vary between 0.086 and 0.211 s (Wagner WE, unpublished data). The stimuli were constructed by digitizing a male
chirp using a Macintosh Ilci computer, a MacRecorder sound
digitizer, and SoundEdit Pro software. A single pulse was selected from this natural chirp and used to construct artificial
chirps (pulse duration = 14 ms, pulse rate of artificial chirps
= 0.038 pulses/ms). First, female preferences based on chirp
rate were tested by giving females a choice between male
songs that varied only in chirp rate. Second, female preferences based on chirp duration were tested by giving females
a choice between male songs that varied only in chirp duration. Third, female preferences based on chirp amplitude
were tested by giving females a choice between male songs
that varied only in amplitude. The amplitude of the high amplitude stimulus was twice that of the low amplitude stimulus.
Fourth, the relative importance of chirp rate and chirp duration was examined. Females were given a choice between a
song of high chirp rate and short chirp duration and a song
of low chirp rate and long chirp duration. The overall acoustic
energy of these stimuli was equal. A preference for the former
stimulus would suggest that chirp rate is more important to
females, while a preference for the latter stimulus would suggest that chirp duration is more important to females. Fifth,
the amplitude dependence of female preferences based on
chirp rate was examined. Females were given a choice between a song of high chirp rate and low chirp amplitude and
a song of low chirp rate and high chirp amplitude. Sixth, the
amplimde dependence of female preferences based on chirp
duration was examined. Females were given a choice between
5
6
High chirp rate
Low chirp rate
Long chirp duration
Short chirp duration
High chirp amplitude
Low chirp amplitude
High rate short duration
Low rate long duration
High rate low amplitude
Low rate high amplitude
Long duration low amplitude
Short duration high amplitude
Chirp Chirp
rate duration
(s)
(/s)
Chirp
amplitude
(dB SPL)'
2
1
2
2
2
2
2
75
75
75
75
75
69
75
75
69
75
69
75
1
2
1
2
2
0.2
0.2
0.2
0.1
0.2
0.2
0.1
0.2
0.2
0.2
0.2
0.1
(100)
(100)
(100)
(100)
(100)
(94)
(100)
(100)
(94)
(100)
(94)
(100)
' Chirp amplitude differed between female cricket and female fly
preference tests. Chirp amplitudes for fly preference tests are given
in parentheses. Amplitude in decibels is re 20 jJ-Pa, measured at a
distance of 1 m from the speaker.
a song of long chirp duration and low chirp amplitude and a
song of short chirp duration and high chirp amplitude.
Female preferences were tested in a 1.22 X 0.61 X 0.31 m
(1 X w X h) wooden arena. The sides were covered with foam
to improve the localizability of broadcast sound. A Realistic
40-1259A amplified speaker was placed at each end of the
arena. A 40 watt red light allowed observation of females within the arena. Prior to a test, a female was placed under an
opaque plastic dish equidistant between the speakers and allowed to acclimate for 10 min. A small piece of cardboard egg
carton provided shelter for the female. A pair of stimuli were
then broadcast from a Toshiba KT-4529 personal cassette player through the speakers; the stimuli were recorded on different tracks, and each stimulus was broadcast through a different speaker. Stimulus amplitudes were adjusted prior to the
beginning of each test using a Realistic Sound Level Meter.
The dish was removed and the female was observed until she
contacted one of the speakers, at which time a choice was
considered to have occurred. Some females failed to respond
after 20 min. These females were removed from the arena
and were retested on a subsequent night Between the tests,
the stimuli were switched between speakers to control for potential side biases. To determine whether females preferred
one alternative stimulus over another, the number of females
selecting each stimulus was compared with a two-tailed binomial test (Sokal and Rohlf, 1981). Females that continued to
respond were occasionally tested with more than one pair of
stimuli within a night. Most females were tested on more than
one night, although each female was tested only once with a
given pair of stimuli. All tests were conducted between 18.3°C
and 19.8°C (x = 19.1°C). The chirp rate and chirp duration
stimuli fall within the natural range of variation for males calling at this temperature (Wagner WE, unpublished data).
Preferences of parasitoid flies
The influence of variation in male singing behavior on fly
attraction was tested in the field from 18 September to 7 October 1992 at Tucker's Grove County Park. Two Realistic 401259A amplified speakers were placed 1 m apart at the edge
of a dirt and grass clearing from which male G. lineaticeps had
previously called. During the experiments no calling males
were within 40 m of the speakers (any males present were
relocated). Alternative stimuli were then broadcast through
Wagner • Convergent song preferences
Test
281
Stimuli
Number of
female crickets
Number of
female flies
(a)
High chirp rate
13**
23**
12*
19*
12*
20**
Low chirp rate
(b)
Long chirp duration
Short chirp duration
(c)
High chirp amplitude
Low chirp amplitude
* P < 0.05, • • P < 0.01, *•• P < 0.001
the speakers from a Toshiba KT-4529 personal cassette recorder. The stimuli used were the same as those used to examine female cricket preferences (see above), except that the
stimuli were broadcast at a higher amplitude (Table 1). The
higher amplitudes were used to maximize the area over which
the songs were detectable by flies to increase the number of
flies attracted to the playbacks. Playbacks were started approximately 15 min prior to sunset, and continued until approximately 45 min after sunset. O. ochracea approach broadcast
song primarily in the period shortly before and after sunset.
All tests were conducted between 17.3°C and 21.8°C (x =
18.5°C).
In response to the song playbacks, female flies either landed directly on one of the speakers or landed within 40 cm of
a speaker and walked toward it. Once in contact with a speaker, flies generally moved over the surface of the speaker, apparently searching for the calling male cricket. Flies that contacted a speaker were collected and counted. To determine
whether flies preferred one type of song to another, the number of flies landing on each speaker was compared with a twotailed binomial test. Most of the experiments were conducted
over a number of nights (x = 2.0 nights, SE = 0.26). Stimuli
were switched between speakers between nights to help con-
Figure 2
The preferences of female
field crickets (G. lineaticeps)
and female tachinid flies (O.
ockracea) based on variation in
(a) chirp rate, (b) chirp duration, and (c) chirp amplitude
of male calling song. The number of female field crickets and
female tachinid flies attracted
to each stimulus is compared
with a two-tailed binomial test
trol for potential position effects. In addition, collected flies
were preserved to prevent individual flies from responding in
the same test both within and between nights.
RESULTS
Single song characters
Chirp rate, duration, and amplitude all influenced female
mate choice and the probability of fly attraction. When presented with songs that varied only in chirp rate, significantly
more female crickets and female flies were attracted to the
higher chirp rate song (Figure 2a). When presented with
songs that varied only in chirp duration, significantly more
female crickets and female flies were attracted to the longer
chirp duration song (Figure 2b). And when presented with
songs that varied only in chirp amplitude, significantly more
female crickets and female flies were attracted to the higher
chirp amplitude song (Figure 2c). These results suggest that
female C. lineaticeps prefer higher chirp rates, longer chirp
durations, and higher chirp amplitudes. These results also
suggest that males with these call characters have a higher risk
of attracting parasitoid flies.
Behavioral Ecology Vol. 7 No. 3
282
Test
Stimuli
Number of
female crickets
Number of
female flies
(a)
Long chirp duration
Low chirp rate
22
Short chirp duration
High chirp rate
19
(b)
High chirp rate
Low chirp amplitude
-HttHH
13**
Low chirp rate
High chirp amplitude
Figure 3
The preferences of female
field crickets (G. lineaticeps)
and female tachinid flies (O.
ochracea) based on (a) simultaneous variation in chirp rate
and chirp duration, (b) simultaneous variation in chirp rate
and chirp amplitude, and (c)
simultaneous variation in chirp
duration and chirp amplitude
in male calling song. The number of female field crickets and
female tachinid flics attracted
to each stimulus is compared
with a two-tailed binomial test.
38*
21
(c)
Long chirp duration
Low chirp amplitude
15*
26**
Short chirp duration
High chirp amplitude
* P < 0.05, •* P < 0.01, *** P < 0.001
Multiple song characters
Chirp rate and chirp duration did not appear to differ in their
relative importance to female crickets and female flies. Two
songs were presented that simultaneously varied in chirp rate
and chirp duration: one song contained chirps 100 ms in duration at a rate of 2 chirps/s while the other song contained
chirps 200 ms in duration at a rate of 1 chirp/s. The acoustic
energy of the two songs was thus equal. The number of female
crickets and the number of female flies attracted to each song
type did not significantly differ (Figure 3a).
The influence of variation in chirp rate and chirp duration
on both female mate choice and the probability of fly attraction were at least partially independent of chirp amplitude.
When presented with songs of 2 chirps/s and 1 chirp/s, where
the amplitude of the former was half that of the latter, significantly more female crickets and female flies were attracted
to the high chirp rate/low chirp amplitude song (Figure 3b).
The number of female crickets and female flies attracted to
the high versus low chirp rate song did not significantly differ
from the experiments where chirp amplitude was constant (female crickets: G = 0.00, df = 1, p = 1.00; female flies: G =
2.12, df = 1, p > .20). Similarly, when presented with songs
with chirps of 200 ms and 100 ms, where the amplitude of the
former was half that of the latter, significantly more female
crickets and female flies were attracted to the long chirp duration/low chirp amplitude song (Figure 3c). The number of
female crickets and the number of female flies attracted to
the long versus short chirp duration song did not significantly
differ from the experiments where chirp amplitude was constant (female crickets: G = 0.12, df = 1, p > .90; female flies:
G = 1.61, df = 1, p > .40). These results suggest that variation
in chirp amplitude does not have a major effect on the preferences of female crickets and female flies based on other
chirp characteristics.
DISCUSSION
Sexual and natural selection on male calling song
G. lineaticeps calling songs with higher chirp rates and longer
chirp durations were more likely to attract both conspecific
females and parasitoid flies (O. ochracea). The song preferences of female G. lineaticeps are similar to those of other
crickets where females prefer longer calls or calls produced
at a more rapid rate (e.g., Hedrick 1986; Pollack and Hoy,
1981; Popov and Shuvalov, 1977; Stout and McGhee, 1988;
Wagner et al., 1995). While female flies are known to discrim-
Wagner • Convergent song preferences
283
and Ryan, 1981). Similarly, in G. lineaticeps, sexual selection
inate between the calling songs of different species of cricket
by female choice and natural selection by fly predation should
(Walker, 1986, 1993), little is known about the preferences of
have opposing effects on the evolution of male singing befemale flies based on intraspecific variation in song structure.
havior.
Both female crickets and female flies preferred higher
chirp amplitudes. Because the amplitude of a chirp at any
given location will depend primarily on the distance of the
The evolution of female mating preferences
male producing the chirp, these results suggest that female
crickets and female flies prefer closer males. Mating preferFemale mating preferences can evolve because of Fisherian
ences based on amplitude are common in species where feprocesses (Kirkpatrick, 1982; Lande, 1981), because of assomales select mates based on acoustic signals (Gerhardt, 1991;
ciations between female preferences and female fitness (reRyan and Keddy-Hector, 1992; Walker and Forrest, 1989), but
viewed by Kirkpatrick and Ryan, 1991; Thorn hill and Alcock,
little is known about the amplitude preferences of acoustically
1983), because of differences between males in heritable comorienting predators. These results are not surprising, however,
ponents of fitness (Grafen, 1990; Kirkpatrick, 1987a; Pomiangiven that higher chirp amplitudes often mean shorter travel
kowski, 1987; Zahavi, 1975), or because of evolutionary prodistances, and given that search costs are expected to influcesses independent of sexual selection on the trait in question
ence both female preferences (Kirkpatrick, 1987a; Pomian(Basolo, 1990; Endler and McClellan, 1988; Kirkpatrick,
kowski, 1987; Real, 1990) and foraging behavior (e.g., God1987b; Ryan, 1990). In contrast, search costs associated with
fray, 1994; Stephens and Krebs, 1986). Despite these preferfemale preferences are expected to favor less discriminating
ences for higher amplitude chirps, when presented with songs
females (Kirkpatrick, 1987a; Maynard Smith, 1991; Pomianof high and low chirp rate, where the high chirp song rate
kowski, 1987).
was of lower amplitude, both female crickets and female flies
The reason female G. lineaticeps prefer higher chirp rates
preferred the higher chirp rate song. Similarly, when preand longer chirp durations is not known. In some crickets
sented with songs of long and short duration, where the long
song characters preferred by females may be indicative of largchirp duration song was of lower amplitude, both female
er male size (e.g., Simmons, 1988), and larger male size may
crickets and female flies preferred the longer chirp duration
be indicative of greater material benefits or higher fitness. In
song. These results suggest that female crickets and female
G. lineaticeps, however, neither chirp rate nor chirp duration
flies will often bypass closer males producing less preferred
is correlated with male size (Wagner WE, unpublished data).
songs in favor of more distant males producing more preFemale choice based on these characters thus will not result
ferred songs.
in matings with larger males. It is not known whether chirp
amplitude is correlated with male size. However, because variSome male traits may be more important than others both
ation in chirp amplitude will primarily result from variation
to conspecific females and to eavesdropping predators (e.g.,
in male distance and variation in male position relative to a
Gerhardt, 1991; Wells and Taigen, 1986). However, neither
female (i.e., inside or outside a burrow), it seems unlikely that
female crickets nor female flies discriminated between high
female choice based on this character will generally result in
chirp rate/short chirp duration song and low chirp rate/long
matings with larger males (but see Arak, 1988).
chirp duration song. There is thus no evidence that these
traits differ in their importance to either female crickets and
In many animals, females prefer more energetic displays
female flies, although differences still might exist in the rel(Ryan and Keddy-Hector, 1992). Because males with higher
ative importance of chirp rate and chirp duration to individchirp rates and longer chirp durations produce songs conuals of both groups.
taining greater acoustic energy, it is possible that female G.
lineaticeps simply prefer more conspicuous song, either beFemale crickets often have the opportunity to exercise mate
cause such song results in greater neural stimulation or bechoice under natural conditions (Loherand Dambach, 1989).
cause such song is easier to localize. However, in tests where
Because females preferred higher chirp rates and longer
the acoustic energy contained in male calls was controlled,
chirp durations, directional sexual selection should favor
higher chirp rates and longer chirp durations in G. lineaticeps. females preferred higher chirp rates and longer chirp durations despite these song types being of lower amplitude. These
It is possible that measurable preferences may not result in
results suggest that females do not simply prefer songs of
sexual selection on the preferred male trait, even when fegreater energy, but instead prefer higher chirp rates and lonmales have the opportunity to exercise mate choice (e.g.,
ger chirp durations per se; because a song that is half the
Wagner and Sullivan, 1995). However, female preferences ofamplitude of another song is generally twice as far away, feten result in sexual selection if females have the opportunity
males appear willing to travel at least twice as far to mate with
to exercise mate choice (reviewed by Andersson, 1994; Kirka male producing a preferred song type. The reason that fepatrick, 1987b; Searcy and Andersson, 1986).
males prefer males with higher chirp rates and longer chirp
Previous work on field crickets has suggested that fly predurations
remains to be determined. Possibilities include redation has influenced the evolution of noncalling, satellite
duced search costs due to ease of localization, male genetic
behavior in male field crickets (Cade, 1975, 1979), the evoquality (Grafen, 1990; Heywood, 1989; Pomiankowski, 1988;
lution of a reduced nightly duration of male calling (Cade
Zahavi, 1975), spermatophore quantity or quality (Zuk, 1987),
and Wyatt, 1984; Zuk et al., 1993), and evolutionary changes
and avoidance of transmissible parasites (Borgia and Collis,
in calling song structure (Zuk et al., 1993). The expression of
1990).
song preferences by female flies likewise suggests that fly predation will have an important consequence for male singing
behavior; fly predation should result in selection against higher chirp rates and longer chirp durations in G. lineaticeps call- The evolution of fly preferences
ing song. In other species predation is known to counter sexFemale O. ochracea show extensive geographic variation in
ual selection by female choice. In guppies (Poedlia reticulata), their hosts. In central Texas they utilize G. integer (Cade,
females prefer males with red coloration, a trait that increases
1975), in Florida they utilize G. rubensand G. firmus (Walker,
a male's probability of being eaten by a predator (Endler,
1986; Walker and Wineriter, 1991), m California they utilize
1980, 1982). In a frog (Physalaemus puslulosus), females pre- G. lineaticeps (this article), and in Hawaii, where the fly apfer males that produce chucks, a behavior that increases a
pears to have been introduced, they utilize an introduced
male's risk of being eaten by acoustically orienting bats (Tuttle
field cricket, Teleogryllus oceanicus (Zuk et al., 1993). A num-
284
ber of observations suggest that there are evolved differences
between populations in the responses of O. ochracea to cricket
calling song. In central Texas, flies respond readily to the
trilled calling song of G. integer (Cade, 1975), but in Florida,
where C. integer does not occur, they rarely respond to G.
integer song (Walker, 1993). In Florida, flies respond readily
to the trilled calling song of G. rubens but rarely respond to
the chirped calling song of G. firmus (Walker, 1993). In contrast, flies readily respond to the chirped calling song of G.
lineaticeps in California (this article) and of T. oceanicus in
Hawaii (Zuk et al., 1993).
As the results presented here illustrate, female O. ochracea
not only discriminate between the songs of potential host species, but they also discriminate between song types within a
given host species. The reason that female O. ochracea prefer
G. lineaticeps song of higher chirp rate and longer chirp duration is currently unclear. In general, the factors influencing
the evolution of host preferences in O. ochracea should be
similar to those that influence foraging behavior in other animals, including other parasitoids, such as search costs and
food or host profitability (reviewed by Godfray, 1994; Stephens and Krebs, 1986). First, higher chirp rates and longer
chirp durations may be easier for flies to localize, even when
such songs are of much lower amplitude. Female flies may
thus minimize their search costs by orienting to such songs.
Second, male crickets producing higher chirp rates and longer chirp durations may be better hosts for a female fly's larvae. For example, males producing higher chirp rates and
longer chirp durations may be in better physiological condition, and male crickets in better physiological condition may
be more likely to survive until larval emergence, may be capable of supporting more larvae, and may provide more resources for each larva, resulting in larger or more viable larvae. Third, the presence of larvae in a male may affect male
singing behavior, as it is known to affect other aspects of male
behavior (Adamo et al., 1995a; Cade and Wyatt, 1984). If larvae deposited on a previously infested male have a reduced
probability of successful emergence or reduced pupal size
(e.g., Adamo et al., 1995b), the preferences of female flies
may enhance offspring survivorship or fitness. Fourth, males
with higher chirp rates and longer chirp durations may be
more likely to have conspecific females within or near their
burrows. Female flies may prefer such males because there is
a higher probability that two or more hosts will be present
rather than one (e.g., Walker and Wineriter, 1991). Host preferences based on host quality are common in animals (see
Godfray, 1994), and female flies may prefer some song types
because they provide information about a male cricket's suitability as a host or information about the number of hosts
that may be present.
I thank the Santa Barbara Parks and Recreation Department for permission to conduct research in Tucker's Grove County Park, and J.
A. Endler for use of his laboratory. I also thank A. L. Basolo, W. H.
Cade, D. W. Leger, D. J. Mountjoy, A.-M. Murray, L. W. Simmons, T.
J. Walker, and an anonymous reviewer for their criticism of the manuscript. The research was supported by North Atlantic Treaty Organization and National Science Foundation postdoctoral fellowships.
Preparation of the manuscript was supported by the National Science
Foundation's Experimental Program to Stimulate Competitive Research, through funding of the Nebraska Behavioral Biology Group.
REFERENCES
Adamo SA, Robert D, Hoy RR, 1995a. Effects of a tachmid parasitoid,
Ormia ochracea, on the behaviour and reproduction of its male and
female field cricket hosts (GryUus spp). J Insect Physiol 41:269-277.
Adamo SA, Robert D, Perez J, Hoy RR, 1995b. The response of an
insect parasitoid, Ormia ochracea (Tachinidae), to the uncertainty
Behavioral Ecology Vol. 7 No. 3
of larval success during infestation. Behav Ecol Sociobiol 36:111118.
Alexander RD, 1961. Aggressiveness, territoriality, and sexual behavior
in field crickets (Orthoptera: Gryllidae). Behaviour 17:130-223.
Andersson M, 1994. Sexual selection. Princeton: Princeton University
Press.
Arak A, 1988. Female mate selection in the natterjack toad: active
choice or passive attraction? Behav Ecol Sociobiol 22:317-327.
Basolo AL, 1990. Female preference predates the evolution of the
sword in swordtail fish. Science 250:808-810.
Borgia G, Collis K, 1990. Parasites and bright male plumage in the
satin bowerbird (Ptilonorhynchus violaceus). Am Zool 30:279—285.
Cade WH, 1975. Acousucally orienting parasitoids: fly phonotaxis to
cricket song. Science 190:1312-1313.
Cade WH, 1979. The evolution of alternative male reproductive strategies in field crickets. In: Sexual selection and reproductive competition in insects (Blum MS, Blum NA, eds). New York: Academic
Press; 343-379.
Cade WH, Wyatt DR, 1984. Factors affecting calling behaviour in field
crickets, TeUogryUus and GryUus (age, weight, density, and parasites). Behaviour 88:61-75.
Darwin C, 1871. The descent of man, and selection in relation to sex.
London: Murray.
Endler JA, McLellan T, 1988. The processes of evolution: towards a
newer synthesis. Annu Rev Ecol Syst 19:395—421.
Endler JA, 1980. Natural selection on color patterns in Poectlia retxculata. Evolution 31:78-91.
Endler JA, 1982. Convergent and divergent effects of natural selection
on color patterns in twofishfaunas. Evolution 36:178-188.
Fisher RA, 1958. The genetical theory of natural selection, 2nd rev.
ed. New York: Dover Press.
Gerhardt HC, 1991. Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615-635.
Godfray HCJ, 1994. Parasitoids: behavioral and evolutionary ecology.
Princeton: Princeton University Press.
Grafen A, 1990. Sexual selection unhandicapped by the Fisher process. J Theor Biol 144:473-516.
Hedrick AV, 1986. Female preferences for male calling bout duration
in a field cricket. Behav Ecol Sociobiol 19:73-77.
HeywoodJS, 1989. Sexual selection by the handicap mechanism. Evolution 43:1387-1397.
Kirkpatrick M, 1982. Sexual selection and the evoluuon of female
choice. Evolution 36:1-12.
Kirkpatrick M, 1987a. The evolutionary forces acting on female mating preferences in polygynous animals. In: Sexual selection: testing
the alternatives (Bradbury JB, Andersson MB, eds). Chichesten
John Wiley & Sons; 67-82.
Kirkpatrick M, 1987b. Sexual selection by female choice in polygynous
animals. Annu Rev Ecol Syst 18:43-70.
Kirkpatrick M, Ryan MJ, 1991. The evolution of mating preferences
and the paradox of the lek. Nature 127:403-409.
Lande R, 1981. Models of speciation by sexual selection on polygenic
traits. Proc Nat! Acad Sci USA 78:3721-3725.
Loher W, Dambach M, 1989. Reproductive behavior. In: Cricket behavior and neurobiology (Huber F, Moore TE, Loher W, eds). Ithaca; Cornell University Press; 83-113.
Maynard Smith J, 1991. Theories of sexual selection. Trends Ecol Evol
6:146-151.
Michelsen A, 1985. Environmental aspect of sound communication
in insects. In: Acoustic and vibrational communication in insects
(Kalmring K, Eisner N, eds). Berlin: Paul Parey, 1-9.
PiercyJE, Embleton TFW, Sutherland LC, 1977. Review of noise propagation in the atmosphere. J Acoust Soc Am 61:1403-1418.
Pollack GS, Hoy R, 1981. Phonotaxis to individual rhythmic components of a complex cricket calling song. J Comp Physiol 144:367373.
Pomiankowski A, 1987. The 'handicap principle' does work—sometimes. Proc R Soc Lond B 127:123-145.
Pomiankowski A, 1988. The evolution of female mate preferences for
male genetic quality. Oxford Survey Evol Biol 5:136-184.
Popov AV, Shuvalov VF, 1977. Phonotactic behavior of crickets. J
Comp Physiol 119:111-126.
Price TD, 1984. Sexual selection on body size, territory and plumage
variables in a population of Darwin's finches. Evolution 38:327-341.
Wagner • Convergent song preferences
Real L, 1990. Search theory and mate choice. I. Models of single-sex
discrimination. Am Nat 136:376-405.
Robert D, Amoroso J, Hoy RR, 1992. The evolutionary convergence
of hearing in a parasitoid fly and its cricket host Science 258:11351137.
Ryan MJ, 1985. The Tiingara frog. Chicago: University of Chicago
Press.
Ryan MJ, 1990. Sexual selection, sensory systems, and sensory exploitation. Oxford Survey Evol Biol 7:157-195.
Ryan MJ, Keddy-Hector A, 1992. Directional patterns of female mate
choice and the role of sensor)' biases. Am Nat 139:S4-S35.
Ryan MJ, Tuttle MD, Rand AS, 1982. Bat predation and sexual advertisement in a neotropical frog. Am Nat 119:136-139.
Searcy WA, Andersson M, 1986. Sexual selection and the evolution of
song. Annu Rev Ecol Syst 17:507-534.
Simmons LW, 1988. The calling song of the field cricket, Gryllus btmaculatus (De Geer): constraints on transmission and its role in
intermale competition and female choice. Anim Behav 36:380-394.
Sokal RR, Rohlf FJ, 1981. Biometry, 2nd ed. New York: W. H. Freeman.
Stephens DW, KrebsJR, 1986. Foraging theory. Princeton: Princeton
University Press.
Stout JF, McGhee R, 1988. Attractiveness of the male Acheta domatica
calling song to females. II. The relative importance of syllable period, intensity, and chirp rate. J Comp Physiol 164:277-287.
Sullivan BK, 1987. Sexual selection in Woodhouse's toad (Bufo woodhousei). III. Seasonal variation in male mating success. Anim Behav
35:912-919.
Thornhill R, Alcock J, 1983. The evolution of insect mating systems.
Cambridge: Harvard University Press.
Tuttle MD, Ryan MJ, 1981. Bat predation and the evolution of frog
vocalizations in the neotropics. Science 214:677-678.
Wagner WEJr, Sullivan BK, 1995. Sexual selection in the Gulf Coast
285
toad (Bufo valliceps): female choice based on variable characters.
Anim Behav 49:305-319.
Wagner WEJr, Murray A-M, Cade WH, 1995. Phenotypic variation in
the mating preferences of female field crickets, Gryllus integer.
Anim Behav 49:1269-1281.
Walker TJ, 1957. Specificity in the response of female tree crickets
(Orthoptera: Grylliclae: Oecanthinae) to calling songs of the males.
Ann Entomol Soc Am 50:626-636.
WalkerTJ, 1986. Monitoring the flights of field crickets (Gryllusspp.)
and a tachinid fly (Euphasiopteryx ochracea) in North Florida. Florida Entomol 69:678-685.
Walker TJ, 1993. Phonotaxis in female Ormia ochracea (Diptera, Tachinidae), a parasitoid of field crickets. J Insect Behav 6:389—410.
Walker TJ, Forrest TG, 1989. Mole cricket phonotaxis—effects of intensity of synthetic calling song (Orthoptera, Gryllotalpidae, Scapteriscus acletus). Florida Entomol 72:655-659.
Walker TJ, Wineriter SA, 1991. Hosts of a phonotactic parasitoid and
levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Florida
Entomol 74:554-559.
Weissman DB, Rentz DCF, Alexander RD, Loher W, 1980. Field crickets (Gryllus and Acheta) of California and Baja California, Mexico
(Orthoptera: Gryllidae: Gryllinae). Trans Am Entomol Soc 106:
327-356.
Wells KD, Taigen TL, 1986. The effect of social interactions on calling
energetics in the gray treefrog (Hyla versicolor). Behav Ecol Sociobiol 19:9-18.
Zahavi A, 1975. Mate selection—a selection for a handicap. J Theor
Biol 39:66-82.
Zuk M, 1987. The effects of gregarine parasites, body size, and time
of day on spermatophore production and sexual selection in field
crickets. Behav Ecol Sociobiol 21:65-72.
Zuk M, Simmons LW, Cupp L, 1993. Calling characteristics of parasitized and unparasidzed populations of the field cricket Teleogryllus
oceanicus. Behav Ecol Sociobiol 33:339-343.