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First published online November 17, 2006
Journal of Experimental Biology 209, 4809-4818 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02579
Structure and sexual dimorphism of the electrocommunication signals of the weakly electric fish, Adontosternarchus devenanzii
1 Department of Biology, Indiana University, Bloomington, IN 47405,
USA
2 Center for the Integrative Study of Animal Behavior, Indiana University,
Bloomington, IN 47405, USA
3 Program in Neuroscience, Indiana University, Bloomington, IN 47405,
USA
* Author for correspondence (e-mail: getsmith{at}indiana.edu)
Accepted 3 October 2006
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Summary |
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Key words: communication, sexual dimorphism, electric fish, signal evolution, Adontosternarchus devenanzii
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The electrocommunication signals of weakly electric fish provide an
opportunity to study the mechanisms and evolution of diversity in sexually
dimorphic communication. Both African mormyriform and Neotropical gymnotiform
fishes possess electric organs whose weak electrical discharges function in
electrolocation and communication. The properties of electric organ discharges
(EODs) differ between species and can also vary as a function of sex,
reproductive condition and/or social rank
(Bass, 1986
;
Carlson et al., 2000;
Dunlap and Larkins-Ford, 2003;
Franchina et al., 2001;
Hagedorn and Heiligenberg,
1985; Hopkins,
1988; Kramer et al.,
1980; Zakon and Smith,
2002). Each species produces one of two types of discharge:
pulse-type or wave-type EODs. In pulse-type EODs, the duration of each
discharge is much shorter than the time between discharges, whereas the
duration of each discharge for wave-type EODs is approximately the same as the
time between discharges, resulting in a quasi-sinusoidal signal (reviewed by
Hopkins, 1988;
Moller, 1995).
In species that produce wave-type EODs, the frequency of the discharge
(i.e. number of discharges per second) often differs between the sexes. In
most of the wave-type gymnotiform fish that have been studied, males emit
lower frequency EODs than females (Dunlap
and Zakon, 1998; Hagedorn and
Heiligenberg, 1985; Hopkins,
1974b). Interestingly, however, in the most speciose gymnotiform
family, the Apteronotidae, sex differences in EOD frequency have been studied
in only three species in a single genus, and the direction of sexual
dimorphism differs between these species. In the black ghost knifefish
(Apteronotus albifrons), males produce EODs at significantly lower
frequencies than females, whereas in two closely related species commonly
called brown ghost knifefish (Apteronotus leptorhynchus and
Apteronotus rostratus), EOD frequency is higher in males than females
(Dunlap et al., 1998;
Hagedorn and Heiligenberg,
1985; Kolodziejski et al.,
2005; Meyer et al.,
1987). Although the hormonal mechanisms underlying this reversal
in the direction of sexual dimorphism in EOD frequency have been studied
(Dunlap et al., 1998), the
function of males having higher versus lower EOD frequency than
females in apteronotids is not known.
Another type of electrocommunication signal, chirping, also differs across
species and between sexes. Wave-type EODs are continuously emitted at precise
frequencies that can indicate species, sex and/or rank. When fish interact,
however, they can also transiently modulate the frequency and/or amplitude of
their EODs to produce different types of signals known as chirps, gradual
frequency rises (GFRs) and interruptions
(Dye, 1987;
Hagedorn and Heiligenberg,
1985; Hopkins,
1974b; Larimer and MacDonald,
1968). In A. leptorhynchus, chirping is highly sexually
dimorphic, with males chirping more than females
(Dunlap et al., 1998;
Kolodziejski et al., 2005;
Zupanc and Maler, 1993). By
contrast, the amount of chirping is not sexually dimorphic in A.
albifrons (Dunlap and Larkins-Ford,
2003; Dunlap et al.,
1998; Kolodziejski et al.,
2005).
The structure of chirps [i.e. the duration and degree of amplitude and
frequency modulation (FM)] also varies between sexes and across species.
Although A. leptorhynchus and A. albifrons both produce
similar types of chirps, the chirps of A. albifrons are approximately
10 times longer in duration than comparable chirp types in A.
leptorhynchus (Dunlap and
Larkins-Ford, 2003;
Kolodziejski et al., 2005).
High-frequency chirps (i.e. chirps with more than 150 Hz of FM) are produced
more often by males than females in both species, and the amount of FM and/or
duration of chirps is also sexually dimorphic
(Dunlap and Larkins-Ford, 2003;
Dunlap et al., 1998;
Hagedorn and Heiligenberg,
1985; Kolodziejski et al.,
2005).
Thus, the closely related apteronotid species whose electrocommunication
signals have been well-studied differ in the degree and/or direction of sexual
dimorphism in EOD frequency and chirping. Since more than 60 apteronotid
species in 14 genera have been identified
(Crampton and Albert, 2006) and
because electrocommunication signals can be easily recorded and quantified,
this family offers an unusual opportunity to investigate the evolution of
sexually dimorphic communication. To take advantage of this species diversity,
however, the communication signals of apteronotid fish in genera other than
Apteronotus must be studied. We further characterized the diversity
of electrocommunication signals by examining the structure of chirps and sex
differences in EOD frequency and chirping in Adontosternarchus
devenanzii, an apteronotid species in a genus with numerous derived
characters, including intraspecific diversity in EOD waveform and the presence
of accessory electric organs (Bennett,
1971; Crampton and Albert,
2006).
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Materials and methods |
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) (11
males and 10 females) were purchased from a reputable commercial supplier
(Rose Tropical Fish, Miami, FL, USA) and were housed in 65 l or 34 l tanks
maintained at 26-27°C, pH 5.5-6.5 and conductivity of 100-500 S
cm-1. Experiments complied with the National Institutes of Health
Guide for the Care and Use of Laboratory Animals and protocols
approved by the Indiana University Animal Care and Use Committee. A.
devenanzii is not sexually dimorphic in body size or external morphology,
and we were therefore unaware of the sex of each fish when its
electrocommunication behavior was recorded. The sex of most fish was
determined later by laparotomy. After behavioral testing was completed, fish
were anesthetized with 0.075% 2-phenoxyethanol. A small incision was made in
the ventral body wall, and the gonads were examined to determine the sex of
the fish. The incision was sutured with 8-0 silk and sealed with Nexaband
surgical tissue adhesive (Abbott Laboratories, North Chicago, IL, USA). One
male and one female died after the study, and two males and two females were
killed after their behavioral recordings for use in a separate
immunohistochemical study. The sex of these fish was determined by post-mortem
examination of the gonads. In these cases, gonads were removed and weighed,
and reproductive condition was estimated by calculating the gonadosomatic
index (GSI, gonad massx100/body mass). Some of the fish (five males and
six females) were weighed to the nearest 0.1 g to test for sex differences in
body mass and/or correlations between size and EOD frequency or chirping.
Recording electrocommunication behavior
The EOD frequency of each fish was measured by placing a shielded pair of
wires next to the tail, amplifying the voltage between those wires
(100x; model P-55; Grass Instruments, W. Warwick, RI, USA) and using the
frequency counter of a digital multimeter (Fluke model 187, Everett, WA, USA).
The temperature of the water was also measured to the nearest 0.1°C, and a
Q10 of 1.8 was used to correct each EOD frequency measurement to
that expected at 26.0°C (Dunlap et
al., 2000).
EOD modulations were recorded and analyzed by using methods described
previously (Kolodziejski et al.,
2005). Briefly, fish were placed in a PVC tube with plastic mesh
over both ends and a mesh-covered window midway down the length of the tube.
The tube was placed in the center of a 37 l aquarium maintained at
25.8-27.0°C and at the conductivity and pH of the fish's home tank. The
fish were allowed to acclimate to the recording tank for 1 h. A pair of carbon
electrodes placed at the fish's head and tail recorded its EOD, and a second
pair of electrodes on either side of the tube was used to present playback
stimuli. The signal from the recording electrodes was band-pass filtered (0.1
Hz-10 kHz), amplified (100-1000x; Grass model P-55) and digitized at
44.1 kHz on the left channel of a sound card in a computer running Cool Edit
Pro (Syntrillium, Phoenix, AZ, USA). Playback stimuli were sinusoidal voltage
signals generated by a function generator (Model GFG-8216A or GFG-8219A;
Instek, Chino, CA, USA) and calibrated to a root-meansquare field amplitude of
1.5 mV cm-1 parallel to the stimulating electrodes and midway
between them. This amplitude approximates that of the EOD of a medium-sized
A. devenanzii. A copy of the stimulus was digitized on the right
channel of the sound card. A 4-min baseline recording was made from each fish
without stimulation, and five recordings were made with different playback
stimuli. Each recording consisted of a 1-min baseline period with no
stimulation, two minutes of playback stimulation and 1 min post-stimulus. The
frequencies of the playback stimuli were set relative to the fishes' own EOD
frequencies: 150 Hz above and below the EOD frequency (±150 Hz), 20 Hz
above and below the EOD frequency (±20 Hz) and 5 Hz below the EOD
frequency (-5 Hz). The playback frequencies spanned the species-typical range
of EOD frequencies and were meant to simulate the presence of a conspecific
fish in the recording tank. Based on results in other apteronotid fish, we
expected the -5 Hz stimulus to evoke a jamming avoidance response (JAR)
(Bullock et al., 1972). Stimuli
were presented in random order and were separated by 10-min intervals without
stimulation.
Analysis of EOD modulations
We used a customized procedure written by Brian Nelson (University of
Oregon, Eugene, OR, USA) and running in Igor Pro (Wavemetrics, Lake Oswego,
OR, USA) to calculate EOD frequency and to count and measure the parameters of
EOD modulations (for details, see
Kolodziejski et al., 2005).
Briefly, any playback-induced contamination of the recording was removed by
subtracting an appropriately scaled and phase-shifted copy of the playback
signal. The fundamental frequency of the EOD was calculated by using an
autocorrelation algorithm on 6 ms Hanning windows, advanced 2 ms per
iteration. This process resulted in a temporal resolution of 2 ms and a
frequency resolution of 0.5-3 Hz, depending on the signal-noise ratio of the
recording. The Igor procedure used the mode of EOD frequency in sliding 2 s
windows as a baseline frequency from which to detect EOD modulations. The
procedure counted EOD modulations as any event in which EOD frequency exceeded
this baseline frequency by more than 3 Hz for more than 10 ms and less than 60
s. The beginning and end of each EOD modulation was then defined as the time
at which EOD frequency crossed a threshold of 1 Hz above or below the baseline
frequency. The procedure then calculated the duration and peak frequency of
each modulation. Each EOD modulation was also examined by the experimenter to
confirm that the procedure accurately identified the EOD modulation and
measured its parameters.
Statistics
Body mass, EOD frequency and the numbers and parameters of different types
of EOD modulations were compared between males and females by using unpaired
t-tests. To avoid pseudoreplication, we calculated mean parameter
values (FM and duration) for different EOD modulation types for each fish, and
performed statistical analyses with the mean values for each individual as
independent observations. Repeated measures analysis of variance (RM-ANOVA),
with sex as an independent variable and stimulus frequency as the repeated
measure, was used to determine whether the production of each type of EOD
modulation was influenced by the frequency of the playback stimulus. Since all
fish received the same set of stimuli and stimulus frequency did not affect
the production of EOD modulations (see Results), we analyzed pooled data for
all of the EOD modulations that each individual produced during all six 4-min
recordings (five recordings with stimuli and one baseline recording).
Pearson's correlations were used to test for correlations between body mass
and EOD frequency and numbers of EOD modulations. Results of statistical tests
were considered significant when P<0.05.
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;
Kolodziejski et al., 2005).
Visual inspection of the gonads in the laparotomized fish also demonstrated
that the gonads were well-developed (e.g. yolked follicles were present in
females) and that the reproductive condition of these fish was comparable to
that of the fish whose GSI values were measured. All of the fish were adults,
and total body length for the fish used in this study (180.1-219.0 mm) was at
the top end of the range of lengths recorded in the holotype and paratypes of
A. devenanzii (Mago-Leccia et
al., 1985). The size of males and females overlapped considerably,
and there was no sex difference in body mass
(Table 1,
t9=0.40, P=0.70).
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;
Kolodziejski et al., 2005;
Meyer, 1983), EOD frequency in
A. devenanzii did not differ significantly between males and females
(t19=1.78, P=0.091), although males tended to
have slightly lower EOD frequencies than females
(Table 1). EOD frequency was
not significantly correlated with body mass (r2=0.11,
P=0.33).
Structure and types of EOD modulations
As in other apteronotids, A. devenanzii produced both chirps and
GFRs (Fig. 1). The FM (increase
in EOD frequency) of chirps ranged from 90 to 404 Hz, with most chirps having
100-250 Hz of FM. Chirp durations ranged from 18 ms to 2 s, although most
chirps were 20-150 ms long. GFRs typically had much less FM (3-100 Hz,
interquartile range 4.6-11.1 Hz) and longer and more variable duration (14
ms-15 s, interquartile range 32-264 ms). In A. leptorhynchus and
A. albifrons, chirps can be unambiguously placed into two broad
categories: high-frequency chirps with greater than 150 Hz of FM and
low-frequency chirps with 
30-100 Hz of FM
(Fig. 1B)
(Bastian et al., 2001;
Engler et al., 2000;
Hagedorn and Heiligenberg,
1985; Kolodziejski et al.,
2005). The chirps of A. devenanzii could not be placed
into clear categories based on the amount of FM. The FM of A.
devenanzii chirps was most similar to that of the high-frequency chirps
of A. leptorhynchus and A. albifrons (i.e. typically greater
than 100 Hz of FM), and no low-frequency chirps were produced. Both the chirps
and GFRs of A. devenanzii, however, did vary systematically in
another parameter: the number of frequency peaks. Although some chirps and
GFRs had a single frequency peak, similar to that in most chirps produced by
A. leptorhynchus and A. albifrons, many A.
devenanzii chirps (26.6%) and GFRs (33%) had multiple frequency peaks
(Fig. 1A,E). Most multi-peaked
chirps had 2-4 peaks, although a few had as many as nine peaks. Interestingly,
although multi-peaked chirps typically had greater mean duration than
single-peaked chirps, the duration of single-peaked chirps was more variable
than that of multi-peaked chirps, and the longest chirps were single-peaked
rather than multi-peaked (Fig.
1A,C,D). Unlike the high-frequency chirps of A.
leptorhynchus, but similar to those in A. albifrons, the chirps
of A. devenanzii lacked frequency undershoots (i.e. a decrease in EOD
frequency below its baseline) at the end of the chirp. Similarly, chirps in
both A. devenanzii and A. albifrons had durations several
times longer than those of A. leptorhynchus
(Fig. 1;
Table 1)
(Dunlap and Larkins-Ford, 2003;
Kolodziejski et al.,
2005).
Sex differences in EOD modulations
EOD modulations were sexually dimorphic in A. devenanzii, but
these sex differences were less pronounced than those in A.
leptorhynchus (Table 1;
Fig. 2). Although males tended
to produce more chirps than females, this difference did not reach statistical
significance (t17=2.08, P=0.053). The proportion
of EOD modulations that were chirps (as opposed to GFRs), however, was
significantly greater in males than females; on average, 68.3% of the male EOD
modulations were chirps, compared with only 40% of the female EOD modulations
(t17=2.30, P=0.035). Most of the multi-peaked
chirps were produced by males; males produced more than 12 times as many
multi-peaked chirps as females (t17=2.30,
P=0.035). There were no sex differences in the number of GFRs, and
neither the FM nor the duration of chirps or GFRs differed significantly
between males and females (unpaired t-tests, P>0.15 for
all).
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Effect of stimulus frequency on EOD modulations
A. devenanzii did not chirp differently in response to different
stimulus frequencies (Fig. 3).
Neither the total number of chirps nor the number of multi-peaked chirps was
affected by stimulus frequency (RM-ANOVA, main effect of stimulus frequency,
F4,68=1.27 and 1.02, P>0.29). Consistent with
the unpaired t-test demonstrating that males produced more
multi-peaked chirps, the number of multi-peaked chirps was significantly
affected by sex (RM-ANOVA, F1,17=5.15, P=0.037);
but the interactions of stimulus frequency and sex on the total number of
chirps or multi-peaked chirps were not significant (RM-ANOVA,
F4,68=0.74 and 0.88, P>0.48). Neither sex nor
stimulus frequency affected the number of GFRs or multi-peaked GFRs (RM-ANOVA,
P>0.26 for all factors).
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As in other apteronotid species (Bullock
et al., 1972), the -5 Hz difference frequency stimulus evoked a
JAR. The magnitude of the JAR (i.e. the sustained increase in EOD frequency
caused by the -5 Hz difference frequency stimulus) was not sexually dimorphic
(males 5.48±0.76 Hz, females 5.09±1.11 Hz;
t16=0.30, P=0.77).
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Species diversity in the structure of EOD modulations
The two other apteronotid species whose electrocommunication behavior has
been extensively studied produce three comparable types of EOD modulations
(Kolodziejski et al., 2005).
Both A. leptorhynchus and A. albifrons produce
high-frequency chirps, with more than 150 Hz of FM; low-frequency chirps, with
approximately 20-150 Hz of FM; and GFRs, which have much less FM and more
variable duration. The main difference between the EOD modulations of these
two Apteronotus species is that the chirps of A. albifrons
last 8-12 times longer than those of A. leptorhynchus
(Dunlap and Larkins-Ford, 2003;
Kolodziejski et al., 2005).
A. devenanzii also produced chirps and GFRs, but the chirps of A.
devenanzii could not be categorized as high- and low-frequency chirps.
The FM of A. devenanzii chirps (90-404 Hz) was most similar to the FM
of high-frequency chirps in Apteronotus. Unlike Apteronotus, A.
devenanzii never produced chirps with less than 90 Hz of FM
(Fig. 1A). A.
devenanzii also differed from the other apteronotids in the production of
multi-peaked EOD modulations. Many of the chirps and GFRs in A.
devenanzii had multiple frequency peaks. Although A. albifrons
can produce multi-peaked high-frequency chirps, and A. leptorhynchus
can produce extremely long-duration high-frequency chirps, these modulations
are rare (Dunlap and Larkins-Ford,
2003; Engler and Zupanc,
2001). Similarly, although GFRs in all apteronotids are highly
variable in duration and can have complex FM over time in A.
albifrons (Serrano-Fernandez,
2003), GFRs with multiple sharp frequency peaks like those in
A. devenanzii (Fig.
1E) have not been reported in other apteronotids. The species
differences in chirp parameters suggest that the structure of chirps and GFRs
and the differentiation of chirps into categories have changed during
apteronotid evolution (Fig. 4).
In Apteronotus, distinct chirp types differ mainly in the degree of
FM, whereas in Adontosternarchus chirp categories may be based on
whether they are single- or multi-peaked. Previous studies have hypothesized
distinct functions for different categories of chirps in A.
leptorhynchus, with high-frequency chirps serving as courtship signals,
low-frequency chirps as aggressive signals and GFRs as either submissive
signals or `victory cries' (Bastian et al.,
2001; Dye and Heiligenberg,
1987; Engler and Zupanc,
2001; Hagedorn and
Heiligenberg, 1985;
Serrano-Fernandez, 2003).
Additional comparative studies are needed to determine whether the function,
as well as the structure, of different chirp types varies across apteronotid
species.
Two chirp parameters in A. devenanzii were similar to those in
A. albifrons, but differed from those in A. leptorhynchus.
As in A. albifrons, A. devenanzii chirps lasted several times longer
than most chirps in A. leptorhynchus. In addition, the high-frequency
chirps of both A. devenanzii and A. albifrons lacked
frequency undershoots. These results suggest that short-duration chirps and
frequency undershoots are derived characters in A. leptorhynchus
(Fig. 4). These two parameters
could be mechanistically linked. Chirping is caused by glutamatergic
excitation from the prepacemaker nucleus accelerating the firing rates of
neurons in the pacemaker nucleus, the central pattern generator for the EOD.
It is possible that the rapid removal of excitation needed to produce
short-duration chirps in A. leptorhynchus results in rebound
hyperpolarization in the pacemaker neurons, reducing their firing rate and
leading to a frequency undershoot. Such rebound hyperpolarization might not
occur if the removal of excitation is more gradual, as would be expected for
the longer duration chirps of A. albifrons and A.
devenanzii. Consistent with this hypothesis, A. leptorhynchus
rarely produces extremely long duration high-frequency chirps, which also lack
frequency undershoots [Type 4 chirps of Engler and Zupanc
(Engler and Zupanc,
2001)].
Further studies are needed to investigate the neural mechanisms underlying
species differences in the structure of EOD modulations. In particular, what
aspects of electromotor physiology allow the production of multi-peaked chirps
and GFRs in Adontosternarchus but not Apteronotus? One
possibility is that projection neurons in the prepacemaker nucleus in
Adontosternarchus fire in bursts and excite the pacemaker nucleus in
an oscillatory pattern during EOD modulations, whereas those in
Apteronotus fire tonically. Alternatively, differences in chirp
structure may result from species differences in postsynaptic responsiveness
or intrinsic excitability of neurons in the pacemaker nucleus. For example,
tonic glutamatergic excitation of pacemaker neurons by prepacemaker afferents
might smoothly increase EOD frequency during chirps and GFRs in
Apteronotus but cause oscillating FM in Adontosternarchus.
Dunlap and Larkins-Ford similarly hypothesized that differences between A.
leptorhynchus and A. albifrons in chirp duration might be
mediated by postsynaptic mechanisms in the pacemaker nucleus
(Dunlap and Larkins-Ford,
2003). The ability to study neuronal excitability by using in
vitro preparations of the pacemaker nucleus
(Dye, 1988;
Smith and Zakon, 2000) and
prepacemaker nucleus (G.T.S. and J. A. Kolodziejski, unpublished observations)
will allow these hypotheses to be tested.
EOD waveform and frequency vary considerably across species and may be used
to identify conspecifics (Hopkins,
1974a; Kramer et al.,
1980). The structure of EOD modulations, however, has been
examined in relatively few species (Dunlap
and Larkins-Ford, 2003;
Hagedorn and Heiligenberg,
1985; Hopkins,
1974b; Hopkins,
1974c; Kolodziejski et al.,
2005). Our results and those of other studies suggest that the
structure of EOD modulations may vary as much across species as EOD frequency,
and thus may also convey species-identifying information.
Sex differences in EOD modulations
Sexual dimorphism of chirping varies across apteronotid species. Chirping
is highly sexually dimorphic in A. leptorhynchus. Males chirp 20 to
40 times more than females, and high-frequency chirps are produced almost
exclusively by males (Dunlap et al.,
1998; Kolodziejski et al.,
2005; Zupanc and Maler,
1993). The number of chirps in A. albifrons is not
sexually dimorphic, but chirp structure does differ between the sexes
(Dunlap and Larkins-Ford, 2003;
Dunlap et al., 1998;
Kolodziejski et al., 2005).
Male A. albifrons produce more high-frequency chirps than females,
and male chirps last longer than those of females. As in A.
albifrons, the total number of EOD modulations was not sexually dimorphic
in A. devenanzii, but males and females did differ in the types of
chirps produced. Unlike the Apteronotus species, A.
devenanzii did not produce distinct high- and low-frequency chirps, and
chirps similar to the high-frequency chirps of Apteronotus were
produced by both sexes. Male A. devenanzii, however, produced more
than 10 times as many multi-peaked chirps as females. Thus, multi-peaked
chirps, the electrocommunication signals that are most unique to
Adontosternarchus, are also the most sexually dimorphic signals in
A. devenanzii. This raises the interesting possibility that different
chirp parameters have been sexually selected in different apteronotid
lineages. In Apteronotus, high-frequency chirps are largely
male-specific signals, whereas in Adontosternarchus, multi-peaked
chirps are predominantly produced by males. Future studies examining the
behavioral responses of fish to different types of chirps could test the
hypothesis that the different types of electrocommunication signals produced
mostly by males (i.e. high-frequency chirps in Apteronotus and
multi-peaked chirps in Adontosternarchus) have evolved similar
functions (e.g. courtship). Sexual selection for different signal parameters
in closely related lineages has also been reported for other reproductive
communication signals. For example, different components of song have
diversified through sexual selection in different congeneric songbird species
and in different populations of a ring species
(Irwin, 2000;
Price and Lanyon, 2004).
Sex differences in EOD frequency
We found no significant sex difference in EOD frequency in A.
devenanzii, even though, based on the GSI and the presence of yolked
follicles in females, the fish in this study were sexually mature. EOD
frequencies of males and females overlapped considerably. By contrast, EOD
frequency in other apteronotid species differs markedly between males and
females, with little or no overlap between the sexes
(Dunlap et al., 1998;
Hagedorn and Heiligenberg,
1985; Kolodziejski et al.,
2005; Meyer,
1983). Thus, the four species of apteronotids in which sex
differences in EOD frequency have been examined display three distinct
patterns of sexual dimorphism: (1) males have higher EOD frequencies than
females in A. leptorhynchus and A. rostratus; (2) males have
lower EOD frequencies than females in A. albifrons; and (3) EOD
frequency is not sexually dimorphic in A. devenanzii. The diversity
in the pattern of sex differences in the EOD in the few apteronotid species
studied demonstrates that the direction and magnitude of sexual dimorphism in
EOD frequency is evolutionary labile in this family.
In both Sternopygus and Eigenmannia, non-apteronotid
gymnotiforms that also produce wave-type EODs, EOD frequency is lower in males
than females (Fig. 4)
(Dunlap and Zakon, 1998;
Hagedorn and Heiligenberg,
1985; Hopkins,
1974b; Zakon et al.,
1991). It has thus been hypothesized that ancestral apteronotids
also had males with lower EOD frequencies than females and that the reversal
in the direction of sexual dimorphism of EOD frequency in A.
leptorhynchus and A. rostratus is derived
(Dunlap et al., 1998). Our
results suggest that there may also have been a derived loss of sexual
dimorphism in EOD frequency in the Adontosternarchus lineage
(Fig. 4).
The interspecific variation not only in the presence or absence of sexual
dimorphism of EOD frequency, but also in the direction of sex differences is
unusual. Species differences in the magnitude of sexual dimorphism are common
and may reflect differences in the relative strength of sexual and natural
selection (Andersson, 1994).
Although the direction of sexual dimorphism in body size also often varies
(Fairbairn, 1997), species
differences in the direction of sexual dimorphism in communication behavior,
particularly in the absence of sex-role reversal, are rare. One example occurs
in the parrot, Eclectus roratus, in which greater predation
vulnerability in males and nest-site competition in females have favored
females that are more brightly colored than males despite predominantly female
parental care (Heinsohn et al.,
2005).
Why does both the direction and degree of sexual dimorphism in EOD
frequency vary across apteronotid species? In electric fish that produce
pulse-type EODs, the waveform of the EOD is often sexually dimorphic.
Furthermore, sexual dimorphism of EOD waveform is typically in the same
direction: males have longer duration, higher amplitude and/or more asymmetric
EOD pulses than females (Hopkins,
1999). Sex differences in EOD waveform may be driven by strong
directional sexual selection because the long duration, high amplitude and
asymmetric EOD pulses of males require more energy to produce and/or make
males more conspicuous to both females and electroreceptive predators
(Hopkins, 1999;
Stoddard, 1999;
Stoddard, 2006). The relative
costs and benefits of low-versus high-frequency EODs in wave-type
electric fish are less clear. In fish that produce low-frequency EODs, each
discharge lasts longer and thus may require more energy to produce
(Mills and Zakon, 1987).
However, because fish with low-frequency EODs produce fewer discharges per
second, low-frequency EODs do not necessarily require more overall energy than
high-frequency EODs (Hopkins,
1999). Furthermore, because capacitative coupling in the
neurogenic electric organ of apteronotids strongly attenuates the direct
current (DC) components of the EOD that are detectable by ampullary
electroreceptors (Bennett,
1971), low-frequency EODs are unlikely to be any more or less
conspicuous to electroreceptive predators than high-frequency EODs. If the
costs and benefits of the EOD are not simply related to EOD frequency, the
constraints underlying the directional sexual selection on the EOD in
pulse-type electric fish may be relaxed in apteronotids, allowing
diversification in the direction as well as the magnitude of sex differences
in EOD frequency. Additional studies characterizing sex differences in EOD
frequency in other gymnotiform species and determining whether the direction
or magnitude of these sex differences is correlated with ecological factors
(e.g. mating system, sociality, foraging ecology or predation) are needed to
better understand the factors driving the evolution of sexually dimorphic EOD
frequencies.
The physiological mechanisms underlying species diversity in
electrocommunication behavior also require further investigation. The hormonal
control of sex differences in EOD frequency has been characterized in
Apteronotus. Consistent with the reversal in the direction of sexual
dimorphism, androgens increase EOD frequency in A. leptorhynchus, but
decrease EOD frequency in A. albifrons
(Dunlap et al., 1998). The
effects of hormones on electrocommunication signals in
Adontosternarchus have not yet been studied, but one possible
mechanism that could contribute to the lack of a sex difference in EOD
frequency in this species would be an insensitivity of EOD frequency to
gonadal steroids.
Sexual dimorphism in EOD frequency and differential responsiveness to playbacks
Sex differences in EOD frequency may be associated with responsiveness to
playbacks of different frequencies. A. leptorhynchus produces more
low-frequency chirps, which may function as agonistic signals, in response to
playbacks of frequencies 5-10 Hz away from the fishes' own EOD than to more
distant frequencies (Bastian et al.,
2001; Engler and Zupanc,
2001). Because EOD frequency is sexually dimorphic in A.
leptorhynchus, more low-frequency chirps are thus produced in response to
the EODs of same-sex than opposite-sex individuals. Furthermore, A.
leptorhynchus males produce more high-frequency chirps, which may
function in courtship, to playbacks with frequencies 50-200 Hz away from that
of the male's own EOD (Bastian et al.,
2001; Engler and Zupanc,
2001). Because female EOD frequencies are typically 100-200 Hz
lower than those of males, this behavior results in males producing
high-frequency chirps mostly in response to female EODs. A. albifrons
also chirps differently in response to playbacks of different frequencies (J.
A. Kolodziejski and G.T.S., unpublished observations). By contrast, we found
no effect of stimulus frequency on the number or structure of chirps in A.
devenanzii. The lack of an effect of stimulus frequency on chirping could
be explained by the fact that EOD frequency in A. devenanzii is not
sexually dimorphic and therefore does not convey information about sex. In
both A. leptorhynchus and A. albifrons, sex differences in
EOD frequency make it a reliable cue for directing chirps towards receivers of
one sex or the other. By contrast, because EOD frequency does not differ
between males and females in A. devenanzii, chirping differently to
EODs of different frequencies would not necessarily direct chirps at
individuals based on their sex. If A. devenanzii direct their chirps
in a sex-specific manner, they may use cues other than EOD frequency to assess
the sex of potential receivers.
Apteronotid electrocommunication as a model for studying the evolution of sexually dimorphic behavior
The results of this study and previous studies in other apteronotid species
demonstrate abundant diversity in electrocommunication behavior
(Fig. 4). Phylogenetic
comparative methods to more thoroughly investigate the evolution of this
diversity will require the characterization of sex differences in the
electrocommunication behavior in additional species. The relative ease with
which electrocommunication signals can be elicited and analyzed will
facilitate this process. Furthermore, because electric fish respond robustly
to playbacks with both electrical (e.g. chirping) and physical behaviors (e.g.
by attacking electrodes or depositing eggs near electrodes playing back
conspecific EODs), this system can be used to study the evolution of signal
perception as well as production (Dye,
1987; Hagedorn and
Heiligenberg, 1985; Hopkins,
1974c). Finally, the simplicity of neural circuits that control
both the EOD and its modulations
(Heiligenberg et al., 1996;
Smith, 1999;
Zakon and Smith, 2002) will
allow comparative studies to investigate how sexually dimorphic behaviors and
the physiological mechanisms that control them evolve together.
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Andersson, M. (1994). Sexual Selection. Princeton, NJ: Princeton University Press.
Bass, A. H. (1986). A hormone-sensitive communication system in an electric fish. J. Neurobiol. 17,131 -156.[CrossRef][Medline]
Bastian, J., Schniederjan, S. and Nguyenkim, J.
(2001). Arginine vasotocin modulates a sexually dimorphic
communication behavior in the weakly electric fish Apteronotus
leptorhynchus. J. Exp. Biol.
204,1909
-1923.
Bennett, M. V. L. (1971). Electric organs. In Fish Physiology. Vol. 5 (ed. W. S. Hoar and D. J. Randall), pp. 347-391. New York: Academic Press.
Bullock, T. H., Hamstra, R. H. and Scheich, H. (1972). The jamming avoidance response of high frequency electric fish. I. General features. J. Comp. Physiol. 77, 1-22.[CrossRef]
Carlson, B. A., Hopkins, C. D. and Thomas, P. (2000). Androgen correlates of socially induced changes in the electric organ discharge waveform of a mormyrid fish. Horm. Behav. 38,177 -186.[CrossRef][Medline]
Crampton, W. G. R. and Albert, J. S. (2006). Evolution of electric signal diversity in gymnotiform fishes. In Communication in Fishes. Vol. 2 (ed. F. Ladich, S. P. Collin, P. Moller and B. G. Kapoor), pp.647 -731. Enfield, NH: Science Publishers.
Dunlap, K. D. and Larkins-Ford, J. (2003). Diversity in the structure of electrocommunication signals within the genus of electric fish, Apteronotus. J. Comp. Physiol. A 189,153 -161.[Medline]
Dunlap, K. D. and Zakon, H. H. (1998). Behavioral actions of androgens and androgen receptor expression in the electrocommunication system of an electric fish, Eigenmannia virescens.Horm. Behav. 34,30 -38.[Medline]
Dunlap, K. D., Thomas, P. and Zakon, H. H. (1998). Diversity of sexual dimorphism in electrocommunication signals and its androgen regulation in a genus of electric fish, Apteronotus. J. Comp. Physiol. A 183, 77-86.[CrossRef][Medline]
Dunlap, K. D., Smith, G. T. and Yekta, A. (2000). Temperature dependence of electrocommunication signals and their underlying neural rhythms in the weakly electric fish, Apteronotus leptorhynchus. Brain Behav. Evol. 55,152 -162.[CrossRef][Medline]
Dye, J. (1987). Dynamics and stimulus-dependence of pacemaker control during behavioral modulations in the weakly electric fish, Apteronotus. J. Comp. Physiol. A 161,175 -185.[CrossRef][Medline]
Dye, J. (1988). An in vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish Apteronotus. J. Comp. Physiol. A 163,445 -458.[CrossRef][Medline]
Dye, J. and Heiligenberg, W. (1987). Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish, Apteronotus, during modulatory behaviors. J. Comp. Physiol. A 161,187 -200.[CrossRef][Medline]
Engler, G. and Zupanc, G. K. (2001). Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, Apteronotus leptorhynchus. J. Comp. Physiol. A 187,747 -756.[CrossRef][Medline]
Engler, G., Fogarty, C. M., Banks, J. R. and Zupanc, G. K. (2000). Spontaneous modulations of the electric organ discharge in the weakly electric fish, Apteronotus leptorhynchus: a biophysical and behavioral analysis. J. Comp. Physiol. A 186,645 -660.[CrossRef][Medline]
Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annu. Rev. Ecol. Syst. 28,659 -687.[CrossRef]
Franchina, C. R., Salazar, V. L., Volmar, C.-H. and Stoddard, P. K. (2001). Plasticity of the electric organ discharge waveform of male Brachyhypopomus pinnicaudatus. II. Social effects. J. Comp. Physiol. A 187,45 -52.[CrossRef][Medline]
Hagedorn, M. and Heiligenberg, W. (1985). Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim. Behav. 33,254 -265.[CrossRef]
Heiligenberg, W., Metzner, W., Wong, C. J. H. and Keller, C. H. (1996). Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neural substrate. J. Comp. Physiol. A 179,653 -674.[CrossRef][Medline]
Heinsohn, R., Legge, S. and Endler, J. A.
(2005). Extreme reversed sexual dichromatism in a bird without
sex role reversal. Science
309,617
-619.
Hopkins, C. D. (1974a). Electric communication in fish. Am. Sci. 62,426 -437.[Medline]
Hopkins, C. D. (1974b). Electric communication in the reproductive behavior of Sternopygus macrurus (Gymnotoidei). Z. Tierpsychol. 35,518 -535.[Medline]
Hopkins, C. D. (1974c). Electric communication: functions in the social behavior of Eigenmannia virescens.Behaviour 50,270 -305.
Hopkins, C. D. (1988). Neuroethology of electric communication. Annu. Rev. Neurosci. 11,497 -535.[CrossRef][Medline]
Hopkins, C. D. (1999). Design features for electric communication. J. Exp. Biol. 202,1217 -1228.[Abstract]
Irwin, D. E. (2000). Song variation in an avian ring species. Evolution 54,998 -1010.[CrossRef][Medline]
Kolodziejski, J. A., Nelson, B. S. and Smith, G. T. (2005). Sex and species differences in neuromodulatory input to a premotor nucleus: a comparative study of substance P and communication behavior in weakly electric fish. J. Neurobiol. 62,299 -315.[CrossRef][Medline]
Kramer, B., Kirschbaum, F. and Markl, H. (1980). Species specificity of electric organ discharges in a sympatric group of gymnotoid fish from Manaus (Amazonas). In Sensory Physiology of Aquatic Lower Vertebrates (ed. T. Szabó and G. Czéh), pp. 195-219. Budapest: Akadémiai Kiadó.
Larimer, J. L. and MacDonald, J. A. (1968).
Sensory feedback from electroreceptors to electromotor pacemaker centers in
gymnotids. Am. J. Physiol.
214,1253
-1261.
Mago-Leccia, F., Lundberg, J. G. and Baskin, J. N. (1985). Systematics of the South American freshwater fish genus Adontosternarchus (Gymnotiformes, Apteronotidae). Contrib. Sci. Los Angeles 358,1 -19.
Meyer, J. H. (1983). Steroid influences upon the discharge frequencies of a weakly electric fish. J. Comp. Physiol. A 153,29 -37.[CrossRef]
Meyer, J. H., Leong, M. and Keller, C. H. (1987). Hormone-induced and maturational changes in electric organ discharges and electroreceptor tuning in the weakly electric fish Apteronotus. J. Comp. Physiol. A 160,385 -394.[CrossRef][Medline]
Mills, A. and Zakon, H. H. (1987). Coordination of EOD frequency and pulse duration in a weakly electric wave fish: the influence of androgens. J. Comp. Physiol. A 161,417 -430.[CrossRef]
Moller, P. (1995). Electric Fishes: History and Behavior. London: Chapman & Hall.
Price, J. J. and Lanyon, S. M. (2004). Patterns
of song evolution and sexual selection in the oropendolas and caciques.
Behav. Ecol. 15,485
-497.
Serrano-Fernandez, P. (2003). Gradual frequency rises in interacting black ghost knifefish, Apteronotus albifrons.J. Comp. Physiol. A 189,685 -692.[CrossRef][Medline]
Smith, G. T. (1999). Ionic currents that contribute to a sexually dimorphic communication signal in weakly electric fish. J. Comp. Physiol. A 185,379 -387.[CrossRef][Medline]
Smith, G. T. and Zakon, H. H. (2000). Pharmacological characterization of ionic currents that regulate the pacemaker rhythm in a weakly electric fish. J. Neurobiol. 42,270 -286.[CrossRef][Medline]
Stoddard, P. K. (1999). Predation enhances complexity in the evolution of electric fish signals. Nature 400,254 -256.[CrossRef][Medline]
Stoddard, P. K. (2006). Plasticity of the electric organ discharge waveform: contexts, mechanisms, and implications for electrocommunication. In Communication in Fishes. Vol.2 (ed. F. Ladich, S. P. Collin, P. Moller and B. G. Kapoor), pp. 623-646. Enfield, NH: Science Publisher.
Zakon, H. H. and Smith, G. T. (2002). Weakly electric fish: behavior, neurobiology, and neuroendocrinology. In Hormones, Brain, and Behavior. Vol.2 (ed. D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach, R. Moss and R. Rubin), pp. 349-374. New York: Academic Press.
Zakon, H. H., Thomas, P. and Yan, H.-Y. (1991). Electric organ discharge frequency and plasma sex steroid levels during gonadal recrudescence in a natural population of the weakly electric fish Sternopygus macrurus. J. Comp. Physiol. A 169,493 -499.[Medline]
Zupanc, G. K. H. and Maler, L. (1993). Evoked chirping in the weakly electric fish Apteronotus leptorhynchus - a quantitative biophysical analysis. Can. J. Zool. 71,2301 -2310.
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