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First published online May 18, 2006
Journal of Experimental Biology 209, 2182-2198 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02239
Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes
Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
* Author for correspondence (e-mail: mea21{at}cornell.edu)
Accepted 22 March 2006
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Summary |
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Key words: Mormyridae, playback experiment, Knollenorgan receptor, tuning curve, temporal coding, signal design, multiple EOD dimorphisms
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Introduction |
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), the sensory side of these signaling systems also involves
mate recognition and preference. For example, intersexual selection by mate
choice can play an important role in driving signal divergence and speciation
among populations (Masta and Maddison,
2002; Allender et al.,
2003). It has also been proposed that pre-existing biases in
preferences are involved in the origin of signals within some lineages
(Ryan, 1990;
Endler and Basolo, 1998;
Wilczynski et al., 2001). A
widespread yet currently underappreciated cause of interspecific
diversification in sexually isolating signals and mating preferences involves
species recognition in conjunction with deleterious fitness consequences of
heterotypic or hybrid matings (Servedio
and Noor, 2003). Regardless of the combination of influences that
affects signal divergence, important interactions between the production and
reception sides of communication are expected during the evolution of
signaling systems.
A recently discovered species flock of African mormyrid fishes
(Sullivan et al., 2002) is
well suited for studying signal diversification because its constituent
species exhibit interspecific variation in a relatively simple component of an
electrical communication system. All mormyrid fishes generate brief,
pulse-like electric organ discharges (EODs) by means of an electric organ in
their caudal peduncle (Bennett,
1971a). Different classes of electroreceptors underlie active
electrolocation and communication by detecting the distortions in
self-generated electric fields or the EODs of other individuals, respectively
(Hopkins, 1986;
Kramer, 1990;
Moller, 1995;
von der Emde, 1999). Within
individuals, the sequence of pulse intervals (SPI) between successive EODs
varies rapidly in different electrolocating or social contexts (e.g.
Arnegard and Carlson, 2005). By
contrast, the comparatively fixed waveform of each EOD pulse is shaped by much
slower modifications in the anatomy and physiology of the electric organ
(Bass and Hopkins, 1983;
Bass, 1986;
Caputi et al., 2005). Despite
EOD elongation in breeding males, mormyrids living in species-rich assemblages
are characterized by rather stereotyped, species-typical EODs that are
amenable to quantitative comparison
(Hopkins, 1999;
Arnegard and Hopkins, 2003;
Lavoué et al., 2004;
Feulner et al., 2006). The
largest known radiation of EODs among closely related species occurs in a
riverine species flock from Gabon (Central Africa), members of which have been
assigned to the genus Brienomyrus
(Sullivan et al., 2002).
Sympatric populations of Brienomyrus that differ in appearance and
EOD waveform are reproductively isolated from one another
(Arnegard et al., 2005).
Extensive interspecific signal diversification motivates the hypothesis that
EOD discrimination contributes to species recognition in this group of fishes.
Several behavioral studies have provided strong evidence that mormyrids can
recognize species, sex and/or individuals based on EOD variation
(Hopkins and Bass, 1981;
Graff and Kramer, 1992;
Paintner and Kramer, 2003;
Hanika and Kramer, 2005).
Among the different kinds of electroreceptors possessed by mormyrids,
Knollenorgans are responsible for communication
(Bennett, 1965;
Moller and Szabo, 1981;
Hopkins, 1986;
Bell and Grant, 1989;
Paintner and Kramer, 2003).
The Knollenorgan pathway is briefly inhibited each time a fish fires its own
electric organ, resulting in a selective responsiveness to EODs produced by
other individuals rather than to self-generated EODs
(Zipser and Bennett, 1976;
Mugnaini and Maler, 1987;
Bell and Grant, 1989).
Knollenorgan cells fire spike-like receptor potentials that are time locked to
outside negative-to-positive (N
P) voltage transients
(Bennett, 1971b;
Szabo and Fessard, 1974). When
receptors are activated in nature by an EOD from another fish, Knollenorgans
on opposite sides of an individual's body respond to different phases of the
stimulus. NP transients in one polarity of an EOD waveform experienced
on one side of the body become PN transients in the opposite polarity
waveform experienced on the other side of the body. The result is fixed
latencies between Knollenorgan spiking on opposite sides of the receiver's
body in response to a single EOD. In this way, mormyrids are thought to
distinguish EOD features, such as overall duration, by comparing spike
latencies arising from opposing body regions
(Hopkins and Bass, 1981). Such
a comparison apparently takes place within the midbrain torus semicircularis
(Xu-Friedman and Hopkins,
1999).
An emerging model system for studying sympatric signal diversification
Our study focuses on the magnostipes complex
(Sullivan et al., 2004), which
is nested within Gabon's Brienomyrus species flock and contains three
morphs called types I, II and III (Arnegard
et al., 2005). Similarly sized individuals of co-occurring morphs
cannot be distinguished on the basis of external appearance. Rather, the
morphs are defined by their characteristic EOD waveforms
(Fig. 1). One or two morphs can
be found at each of several sites throughout Gabon
(Fig. 2). Collections made from
the Ivindo River between the middle of September and early December (i.e. at
the beginning of a long, bimodal rainy season) have revealed that mature type
I and type II males are more likely to display elongated EODs during this
period of breeding activity (Fig.
1). At other sites, males and females of a type III morph have
also been collected, although sampling has been insufficient to ascertain the
degree of seasonal waveform elongation by type III males. Wherever the morphs
co-occur, one is always type I; the other can be either type II or type III
(Fig. 2). Measurable
differences in power spectra exist among EODs of the magnostipes
complex (Table 1), yet it is
the time-domain waveform that differs most obviously between sympatric morphs
(Fig. 1). For example, the
first of two major waveform peaks is head-positive in the EOD of type II.
Head-positivity corresponds to current inside the animal flowing in the
direction of the head (i.e. an electrode in the environment near the head is
positive relative to an electrode near the tail). In the case of type I, the
first major peak in the EOD is head-negative. In contrast to other sympatric
mormyrids exhibiting distinctive EODs, reproductive isolation has not been
genetically demonstrated between magnostipes-complex morphs. No
robust differences at five microsatellite loci occur between sympatric morphs
despite their strikingly different EODs. Nevertheless, allopatric populations
of these morphs exhibit signs of strong genetic isolation from one another
(Arnegard et al., 2005).
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The magnostipes complex is a particularly promising system with which to study sympatric signal divergence due to the genetic similarity of co-occurring morphs and the natural replication that exists in the form of multiple dimorphic populations. Knowledge of whether these morphs respond to differences in the EODs they produce is critical to understanding the origins and significance of polymorphism in their electric signals. Here, we report on two sets of experiments in which we tested whether EODs can potentially mediate morph recognition: (1) paired playbacks of female EODs to breeding males; and (2) electrophysiological characterization of Knollenorgan responses to different EOD waveforms.
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Materials and methods |
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500 m wide) and several small tributaries (<10 m wide) within 4
km of the Institut de Recherche en Écologie Tropicale (I.R.E.T.;
Fig. 2). Collections in the
main channel were made at night with worm-baited fish traps or cast nets.
Collections in the tributary streams were made during the day by localizing
individuals with an electrode and oscilloscope and chasing them into handheld
hoop nets. Locations of collection sites are shown in the regional map of
Fig. 2.
We recorded EODs from each specimen in a small aquarium filled with water
from the collection locality (conductivity, 12-28 µS cm-1;
temperature, 21-24°C; pH, 4.5-5.5). Recordings were made as the individual
faced the positive pole of an Ag/AgCl electrode, with the negative pole
positioned posterior to the animal's tail. EODs were amplified using a
low-noise, BMA-831/XR differential bioamplifier (CWE Inc., Ardmore, PA, USA)
and viewed on a Tektronix 222 digital oscilloscope (Tektronix Inc., Beaverton,
OR, USA) to ensure they were not overloaded or otherwise distorted. EODs were
then digitized with a Wavebook (16-bit, 200 kHz; Iotech Inc., Cleveland, OH,
USA) and stored on a portable computer using custom software. As in previous
studies (Arnegard and Hopkins,
2003; Arnegard et al.,
2005), EOD recordings were either DC-(amplifier bandwidth, 0-50
kHz) or AC-coupled (bandwidth, 0.1 Hz-50 kHz). Power spectra of EODs were
estimated using the power spectral density function in Matlab v.6.5.1 (The
MathWorks, Inc., Natick, MA, USA). Immediately after completing both
recordings and playbacks for a given individual (see below), we euthanized it
by administering an overdose of the anesthetic MS222. We measured the
individual's standard length (SL) to the nearest 0.5 mm
(Boden et al., 1997) and
determined its sex and breeding condition by direct gonadal examination.
Specimens were fixed in 10% formalin for two weeks, transferred to 70% ethanol
and deposited in the Cornell University Museum of Vertebrates (cat. nos.
CU89037, 89351-2, 89356-8, 89363-6, 89370, 89373 and 89382-3).
During our collections, we found breeding males and gravid females of each
Ivindo River morph (types I and II). A subset of captured males exhibited
three androgen-dependent character states indicative of breeding condition:
(1) a notchedanal fin base (Herfeld and
Moller, 1998); (2) an elongated EOD waveform
(Bass and Hopkins, 1985); and
(3) an enlarged testis. Many females also proved to be gravid with ripe eggs,
the condition of which was based on limited experience breeding
magnostipes-complex morphs in the laboratory (M.E.A., unpublished).
Compared with the vigorous responses that unconditioned males exhibited to
playback of a wide range of EODs during preliminary trials (e.g. see Results),
unconditioned females appeared relatively unresponsive to electrical
playbacks. Therefore, we focused our experiments on naive male subjects
exhibiting both externally verifiable character states indicative of breeding
activity. An enlarged testis was also subsequently confirmed in each subject
after it was euthanized.
Two-channel playbacks were conducted at I.R.E.T. using clear acrylic chambers like the one shown in Fig. 3. These aquariums were filled with water from the collection locality and provisioned with a central PVC tube shelter. Solitary males were used in experiments soon after capture (i.e. after 24-36 h of acclimation to their chambers). Each male was then simultaneously presented with two digitally synthesized signals consisting of independently controlled EOD waveforms and SPI rhythms (16-bit and down-sampled to 96 kHz). Each signal was played through a different bipolar electrode (Ag/AgCl) situated at each end of the aquarium (Fig. 3). We used an Edirol UA-5 digital playback device (D/A in Fig. 3; Roland Corp., Bellingham, WA, USA) and Cool Edit 2000 software (Syntrillium, Phoenix, AZ, USA) to perform these playbacks. Positive and negative poles of each electrode (oriented parallel to the long axis of the playback aquarium) were separated by 36 mm. Signals from the UA-5 device were amplified using a standard, dual audio power amplifier (LM1877N-9; National Semiconductor, Santa Clara, CA, USA). The output of each channel was isolated using a JT-6110K-B transformer (ISO in Fig. 3; Jensen Transformers, Inc., Van Nuys, CA, USA), which provided an additional 8:1 step-up in voltage. The specified frequency response of the UA-5 device (flat to within -2 dB from 20 Hz-40 kHz) limited the bandwidth of our playback system, which resulted in no detectable distortion of playback EODs.
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To calibrate our system to natural signal amplitudes, we confined an adult
magnostipes-complex female in the tube shelter with fine netting
secured over either end, and we recorded the peak-to-peak amplitude of her EOD
from a bipolar electrode at 20 cm distance. Next, one of the playback
electrodes was identically enclosed in the tube. A previously recorded copy of
the female's EOD was played from either channel of the UA-5 device through
this electrode, and its amplitude was measured at the same distance and
adjusted to approximate that of the live female's EOD. With playback
electrodes positioned as in all trials, the measured peak-to-peak field
strength generated by either calibrated channel was 1.2 mV cm-1 at
the position of the central shelter (water conductivity 27.5 µS
cm-1 for this measurement; central shelter removed; positive and
negative poles of the recording electrode 10 cm apart, rotated parallel to the
aquarium's long axis to give the highest recording amplitude, their bipole
midpoint centered over the shelter's usual position at a distance of 35 cm
from the midpoint of the playback electrode). Open-circuit source potential of
the calibrated test EOD was 19.6 V peak-to-peak, which is slightly less than
that measured for an unloaded electric organ in somewhat larger individuals of
the mormyrid species Gnathonemus petersii
(Bell et al., 1976).
Subsequent to our calibration, the amplitude of one source EOD was slightly
decreased using a custom Matlab routine applied to each pair of playback
signals, such that the sum of squared voltages of each EOD was the same (after
resampling to 96 kHz). This ensured that paired EODs had the same energy
content.
During each playback trial, a male was simultaneously presented with two
EOD waveforms randomly selected from a library of signals recorded in the
Makokou region. In some trials, a homotypic female EOD was presented together
with a heterotypic female EOD (e.g. homotypic and heterotypic EODs played to a
type I male were of types I and II, respectively). In other trials, a
homotypic female EOD was presented with a heterospecific female EOD recorded
from the undescribed sympatric species that has been called the following
names: Brienomyrus sp. `CAB'
(Sullivan et al., 2002;
Arnegard and Hopkins, 2003;
Sullivan et al., 2004;
Arnegard et al., 2005),
Brienomyrus sp. 3 (Alves-Gomes and
Hopkins, 1997; Hopkins,
1999) and Brienomyrus brachyistius `long
biphasic' (l. bp.) (Hopkins,
1981; Bass and Hopkins,
1983; Hopkins,
1986). We adopt the most recent nomenclature for this `reference'
species and hereafter abbreviate its name as `CAB'.
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; Hopkins,
1986; Carlson,
2002). No detailed studies of the patterns and contexts of SPI
production have been made for the magnostipes complex (cf.
Carlson and Hopkins, 2004).
Therefore, no information is available concerning the stereotypy of smooth
accelerations in this complex, nor is anything known about their signaling
function, if any, when produced by a socially isolated individual.
Nevertheless, we opted to use this SPI as our playback rhythm because we
expected a natural SPI to elicit stronger responses than artificial or
scrambled SPIs (Teyssèdre and
Serrier, 1986). For each channel, the timing of EOD presentation
started at a random point in the sequence. The SPI was then independently
looped four times, yielding 2-min presentations per trial with equal total
numbers of energy-normalized EODs for each channel. Only the EOD waveform was
experimentally varied between paired stimuli. Experiments were performed at night (18.30-00.30 h) under infrared illumination provided by two IR lamps (2 W each; Sony model no. HVL-IRC). In each experiment, a male was subjected to four, 2-min playback trials. Each of the two signal pairs outlined above was presented in two trials. The orientation of signal presentation (left versus right) was reversed for the second trial with a given pair of EODs to control for side bias. We randomized the sequence in which the four resulting trials were presented and only started a trial after the male had returned to the central shelter and rested there for at least 60 s. Thus, the male's orientation was perpendicular to each playback bipole at the beginning of a trial (Fig. 3). Water in the playback aquariums was replaced with fresh, aerated water between males.
We videotaped outcomes of all playbacks using a Sony DCR-PC100 digital
video camera. Playback aquariums were outfitted with two recording electrodes
oriented orthogonally to the playback electrodes, which minimizes pick-up of
playback EODs (Fig. 3). Signals
from recording electrodes were amplified and captured in stereo on the audio
tracks of miniDV video tapes (16-bit, 48 kHz). We scored responses of type I
and type II males as either time spent or number of stereotyped bursts of EODs
(e.g. Fig. 4C) produced within
10 cm of a given playback electrode. These bursts were characterized by
constructing SPI plots using a threshold detection approach
(Arnegard and Carlson, 2005).
To facilitate response scoring, we marked playback aquariums with 10-cm
distance thresholds (Fig. 3),
which we arbitrarily determined before beginning any experiments. We summed
scores (either time or number of bursts) over each pair of trials in which the
same set of EODs was played to a given individual. For each morph, we compared
responses to paired EODs using Wilcoxon's signed-ranks tests
(Sokal and Rohlf, 1998). We
used one-tailed tests for these comparisons because we predicted greater
responsiveness to homotypic EODs than to heterotypic or heterospecific EODs
(Ryan and Rand, 1993). We also
estimated the relative magnitude of responsiveness to homotypic EODs as the
simple difference: response to the homotypic EOD minus response to the
heterotypic (or heterospecific) EOD of the same stimulus pair. These relative
response scores were compared between morphs using two-tailed Mann-Whitney
U tests (Sokal and Rohlf,
1998). All statistical tests were performed using Statistica v.6.1
(StatSoft, Inc., Tulsa, OK, USA).
Knollenorgan recordings: tuning characteristics and EOD coding
Upon our return from Africa, we investigated tuning characteristics and
signal-coding properties of Knollenorgan electroreceptors using type I and
type II morphs previously captured from Mouvanga Creek
(Fig. 2). Each individual was
injected with 30 µl of 0.75 mg ml-1 Flaxedil to immobilize it
and eliminate its EOD. A continuous stream of aerated water was passed across
the gills for respiration. We used a previously established approach to
deliver electrical stimuli to Knollenorgans and simultaneously record their
spike-like receptor potentials non-invasively
(Bennett, 1965;
Hopkins and Bass, 1981). To do
so, we used a wire electrode inside a Teflon tube, which we sealed over
individual electroreceptor pores. With Knollenorgans enclosed in this way,
spontaneous firing rates sometimes increased prior to external stimulation
(range, 1.8-300 spikes s-1; mean ± s.e.m., 65±20
spikes s-1). The stimulus artifact was cancelled using a bridge
circuit (Neuroprobe Amplifier, model 1600; A-M Systems, Inc., Carlsborg, WA,
USA), and Knollenorgan spikes were detected using a Schmitt trigger. We used
TDT System 3 hardware (Tucker-Davis Technologies Inc., Alachua, FL, USA) and
custom software developed in Matlab to deliver stimulus waveforms (sampling
rate 50 kHz) to the bridge circuit and record spike times at sub-microsecond
resolution from the Schmitt trigger. Upon the conclusion of each experiment,
the individual was returned to its home aquarium after it recovered from the
Flaxedil.
Stimuli for estimating tuning characteristics of Knollenorgan
electroreceptors consisted of tone bursts (250 Hz-5 kHz), each of which was
played during a 90 ms test window. Tones were ramped on and off using
cosine-squared windows of 5 ms duration before and after each test window. The
number of receptor spikes during the 90-ms test window was compared to the
number of spontaneous spikes in a 90-ms reference window, which began 85 ms
after the test window. The threshold at each frequency was determined by
finding the minimum stimulus amplitude that elicited two more spikes, on
average, in the test window than in the reference window. We also
characterized the response properties of Knollenorgans by obtaining their
reverse correlation (revcor) filters (de
Boer and de Jongh, 1978; Rieke
et al., 1997). To do so, we stimulated each Knollenorgan with
Gaussian white noise and averaged all of the noise segments that immediately
preceded receptor spikes. The resulting average waveform (i.e. the revcor
filter) approximates the linear tuning properties of that receptor; it is
essentially the waveform that best stimulates the receptor. The magnitude
spectrum was calculated for each revcor filter and plotted upside down to
visualize Knollenorgan tuning in the frequency domain. We smoothed each
inverted magnitude spectrum using a three-point, unweighted average before
determining each unit's best response frequency.
Stimuli for examining the coding of EOD waveforms by Knollenorgans
consisted of EODs recorded from the type I, type II and type III morphs from
various regions of Gabon. Knowledge of EOD waveform coding requires
investigation of Knollenorgan responses to both polarities of a stimulus EOD
(Hopkins and Bass, 1981;
Xu-Friedman and Hopkins,
1999). At any given stimulus amplitude, peristimulus time (PST)
histograms of receptor spikes were constructed using data from 300
presentations of an EOD waveform in one polarity (ten EODs per second for 30
s). Knollenorgans were also stimulated with an inverse polarity copy of the
EOD at the same amplitude to construct a second PST histogram. Compound (cPST)
histograms - formed by inverting the second histogram and plotting it together
with the first - were used to qualitatively compare the same unit's response
to different stimulus waveforms. This approach was also used to compare
responses of similarly tuned Knollenorgans between morphs.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Carlson,
2002). These brief bursts were characterized by a sudden drop in
inter-discharge-interval to 8-12 ms, followed by a slower increase to 15-20 ms
or more (Fig. 4C,D). Burst
duration ranged from 200 to 500 ms. While rapidly approaching the electrode,
males often ceased discharging for 0.5-3 s immediately before producing one or
more bursts (e.g. Fig. 4E).
Males only produced bursts during the playbacks and, then, only when they were
within 10 cm of either electrode. Regardless of playback EODs, males typically
approached each electrode multiple times during any 2-min trial, suggesting
that our experimental paradigm effectively presented males with a simultaneous
and sustained `choice' of responding to either signal.
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The type II and type I morphs differed in the relative magnitude of responsiveness to their own (i.e. homotypic) EODs (U=31.0; P=0.0312; two-sided test). When presented with type I and type II EODs simultaneously, type II males displayed on average a greater relative preference for type II EODs (in terms of proximity to the electrodes) than did type I males for type I EODs. The direction of this preference asymmetry was the same for burst production, although the difference was only marginally significant (U=36.0; P=0.0648). No differences were found between morphs in terms of the relative strength of responsiveness to homotypic EODs when these were presented with those of `CAB' (U=63.5 and P=0.8777 for time; U=59.0 and P=0.6666 for bursts; two-sided). In summary, results of the playback experiments rejected the null hypothesis that type II males cannot discriminate magnostipes-complex EODs. They further revealed a difference in responsiveness of type I compared with type II males from the Ivindo River to playback of homotypic versus heterotypic EODs.
Breeding adult size
Given the broad size range of juvenile to adult individuals collected
during past field efforts, we had previously been unable to distinguish
sympatric magnostipes-complex morphs based on body shape or size. In
the present study, we began noticing a tendency for type I breeding males to
be larger than type II breeding males. Therefore, collections of breeding
individuals were increased due to the possible role that a body size
difference might play in the asymmetric responses of males to playbacks.
Breeding males were found to be significantly larger than gravid females
within each morph (Fig. 6;
t37=8.25 and P<0.0001 for type I;
t57=6.50 and P<0.0001 for type II; one-sided
tests). Given the increased sampling, we found a significant difference in
size between Type I and Type II males (Fig.
6; t55=4.97; P<0.0001; two-sided).
Congruent with the result for males, the mean SL of gravid type I females was
larger than that of gravid type II females, but the difference was marginally
insignificant (t39=1.80; P=0.0788; two-sided). In
addition to these comparisons from the Makokou region, the largest few
individuals ever collected in the past from any other location where two
morphs coexist in relatively even numbers
(Fig. 2) have always been type
I males (i.e. 1-3 individuals out of a total of 10-105, depending on
collection locality). This holds true for Mouvanga Creek, the Okano River and
a site at the confluence of the Upper Ogooué and Passa Rivers (M.E.A.,
unpublished), despite the fact that breeding adults were not targeted during
these collections.
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Assuming risk of injury is proportional to opponent size, some portion of the asymmetry in playback responses may be partly explained by the body size difference between morphs and the fact that some full-sized males collected during the breeding season exhibited female-like EODs (M.E.A., unpublished). When presented with type I and type II EODs, the smaller males (type II) spent less absolute time in proximity to type I EODs than did the larger, type I males (Fig. 5; U=38.5; P=0.0453; one-sided Mann-Whitney U test). Despite asymmetries in both male size and unconditioned responsiveness to paired playbacks, the preference of type II males for type II EODs indicates at least some degree of EOD discrimination among genetically indistinguishable sympatric morphs. Given this evidence and what is known about mormyrid electroreception, we expected to find distinct patterns of waveform encoding at the receptor level in response to different EOD types.
Knollenorgan recordings: tuning characteristics and EOD coding
By qualitative comparison to threshold tuning curves, magnitude spectra of
revcor filters (plotted upside down) offer good estimates of Knollenorgan
tuning (e.g. Fig. 7).
Considering revcor filter spectra for all units, Knollenorgans were broadly
tuned in both the type I and type II morphs from Mouvanga Creek
(Fig. 8). Ranges of best
response frequencies were 650-2501 Hz in type I (mean=1180 Hz; N=12)
and 800-5353 Hz in type II (mean=1926 Hz; N=10). Distinct populations
of low-(<1 kHz) and high-(>1 kHz) frequency Knollenorgans have been
reported for Brienomyrus sp. `VAD', which was formerly called
Brienomyrus sp. 2 (Alves-Gomes and
Hopkins, 1997; Sullivan et
al., 2000; Lavoué et
al., 2003) or Brienomyrus brachyistius
`triphasic' (tp.)
(Hopkins, 1983;
Bass and Hopkins, 1984). We
did not record a sufficient number of units to rigorously investigate whether
different populations of Knollenorgans are expressed within the morphs. The
noticeably higher tuning of two units in a single type II individual
(Fig. 8) suggests that such a
division of Knollenorgans might also exist within the magnostipes
complex. Mean best frequencies of all units did not differ significantly
between morphs (t20=1.44; P=0.1646; two-sided),
yet we recognize that the power of this comparison is constrained by our
limited number of samples. Nevertheless, it is worth noting that the mean best
frequency in type II (1125 Hz) was almost identical to that in type I (1180
Hz) after excluding the two highest frequency units.
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P transient in the type I EOD (i.e. the voltage change between
the first and second EOD peaks) dropped to <25 µs, or to within a single
bin of the cPST histogram. However, there were brief delays between slope
maxima of EOD waveforms and corresponding peak spiking times. In response to
some waveform transients, the length of these delays decreased slightly with
increasing stimulus amplitude. Given our non-invasive recording method, we are
unable to report absolute field strengths corresponding to the amplitude
levels provided in Fig. 9. At a given amplitude, we found that a single magnostipes-complex EOD elicited a similar pattern of receptor spiking in both type I and type II individuals when we compared Knollenorgans with similar best frequencies. Furthermore, distinctive patterns of Knollenorgan spiking occurred in response to the different EOD types that characterize the magnostipes complex. Type I EODs of females and non-breeding males caused Knollenorgans to fire one time-locked spike in response to each stimulus polarity (Fig. 9). Knollenorgan responses to elongated EODs of type I breeding males varied depending on the degree to which the stimulus waveforms had elongated and changed (data not shown). Presentation of EODs produced by the type III morph resulted in three or four time-locked spikes (Fig. 9). Two negative peaks in the cPST histogram occurred invariably in response to the inverse polarity presentation of a type III EOD at sufficient amplitude. Either one or two response peaks occurred with positive polarity presentation of a type III EOD, depending on Knollenorgan tuning and stimulus amplitude.
Geographic variation described for type II EODs
(Arnegard et al., 2005) was
reflected in patterns of Knollenorgan response. EODs of the type II morph have
a much smaller initial head-negative peak than those of the type I morph or
the Okano River population of the type III morph. Type II EODs of the Ivindo
River population elicited three preferred spike times at high enough stimulus
amplitudes, with some Knollenorgan spikes locked fairly well to the sharp,
initial head-negative peak (Fig.
9A,B). On the other hand, type II EODs typical of Mouvanga Creek
are characterized by a much broader initial peak (e.g. red traces in
Fig. 9C,D) [see also Arnegard
et al. (Arnegard et al.,
2005)]. Inverse-polarity presentation of these type II EOD
variants resulted in very weak time locking to the broad initial peak but
tight time locking to the largest voltage transient in the waveform
(Fig. 9C,D). Knollenorgan
spikes tended to occur at several temporal positions during positive-polarity
presentation of type II EODs from Mouvanga Creek, due to the relatively slow
transition between the initial head-negative peak and the first head-positive
peak. In the case of both Mouvanga Creek and the Ivindo River, patterns of
Knollenorgan spiking in response to EODs of the type II morph differed from
those elicited by EODs of the alternate co-occurring morph (type I).
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Discussion |
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), discrimination in our behavioral tests would require
Knollenorgans to respond to waveform features that vary among signal classes
of the magnostipes complex.
We found Knollenorgans in type I and type II morphs from Mouvanga Creek to
be broadly tuned and exhibit best frequencies that could not be statistically
distinguished between morphs. The range of best frequencies we estimated
generally encompasses peak-amplitude frequencies of
magnostipes-complex EODs at this site (data not shown), as well as
those of type I and type II morphs elsewhere in Gabon
(Table 1). Any comparably tuned
Knollenorgan in either morph encodes a particular EOD waveform with a similar
pattern of spikes, which are time-locked (with delay) to outside-positive
going (NP) transients in the stimulus waveform. Rather than coding
amplitude, Knollenorgan spikes reliably mark the timing of rapid, and
sufficiently large, voltage changes in the EOD waveform
(Bennett, 1971b;
Hopkins, 1986;
Amagai et al., 1998). In light
of our playback evidence for waveform discrimination, the similarity of
Knollenorgan tuning and EOD encoding between morphs suggests that signal
discrimination can evolve without pre-existing biases at the receptor level
(cf. Ryan, 1990;
Endler and Basolo, 1998;
Wilczynski et al., 2001).
Increasing signal amplitude improves the time locking of Knollenorgan
spikes to EOD waveform features. Compared with mormyromast electroreceptors,
spike-like receptor potentials of Knollenorgans occur at relatively fixed
latencies to suprathreshold stimuli
(Bennett, 1971b;
Szabo and Fessard, 1974).
However, an increase in EOD amplitude can slightly advance the timing of peaks
in Knollenorgan spiking and often changes the relative probability of spiking
at the different response peaks, particularly those corresponding to minor or
gradual waveform features. Electric field strength drops off sharply as the
distance between signaler and receiver increases
(Knudsen, 1975). Therefore,
overt behavioral interactions between mormyrids, such as anti-parallel
displays, in which each of two individuals positions its head as close as
possible to the other individual's electric organ [e.g.
fig. 2 of Bell et al.
(Bell et al., 1974)], may
facilitate encoding of finer waveform features by ensuring high and constant
signal amplitude. The mormyrid morphs in the present study also exhibit
anti-parallel behaviors in certain contexts (M.E.A., unpublished). The
waveform-specific patterns of receptor responses we describe were generated by
averaging over repeated stimulus presentations. Time-coding pathways may
achieve a similar result through convergence and spatial averaging at one or
more levels in the central nervous system (e.g.
Carr et al., 1986). Modest
convergence has already been found at the first central relay of the
Knollenorgan pathway (Bell and Grant,
1989). The possibility of further convergence at the level of
nucleus exterolateralis pars anterior (ELa) warrants consideration.
Within each morph of the magnostipes complex, females and non-breeding males produce similar EODs that are distinctive from those of the other morphs. During the course of the present study, we recorded seasonally elongated EODs from numerous type I and type II males captured from the Ivindo River (Fig. 1). Male EODs in a transitional state of elongation were also encountered. Waveshapes of these transitional EODs resemble shorter-duration EODs produced by females of the same morph, and they grade into the fully altered EODs of males in peak breeding condition. As with females, time-domain EODs of males remain completely distinct between alternate sympatric morphs, despite seasonal waveform changes (Fig. 1). If the receiving individual knows the direction in which the sender is facing (e.g. by means of tactile cues during anti-parallel displays), then differences in receptor responses to EODs of alternate sympatric morphs, whether male or female, become even more obvious than our Knollenorgan recordings might suggest. Type I and type II senders in the same position and orientation often cause the strongest (or most tightly time-locked) Knollenorgan responses to occur on opposite sides of the receiver's body (e.g. Fig. 9C,D).
|
) to all positive
frequencies of its phase spectrum and subtracting the same angle from all
negative frequencies (Heiligenberg and
Altes, 1978; Hopkins and Bass,
1981) (see Fig.
10). Inverse Fourier transformation using the new phase spectrum
yields a temporally altered waveform. A =180° phase shift of this
kind inverts the original EOD (Fig.
10B). Relative to the receiver, inversion of an EOD also occurs
when the sender simply turns and faces the opposite direction. Considering the
range 0°
180° and disregarding sender orientation, a
=90° phase shift maximizes the following measure of deviation,
D[V(t), V(t)],
between the original or reference EOD, V(t), and the
phase-shifted EOD, V(t), over both
polarities of V(t) and all possible temporal alignments
(d) of one waveform to the other:
 |
Here, V and t represent voltage and time, respectively,
and both waveforms are assumed to be sampled at the same rate. As illustrated
in Fig. 10B,C (left column), a
=90° transformation of the kind described results in the largest
alteration in time-domain structure of any given EOD. Characteristic EODs of
breeding males do not vary noticeably in amplitude spectra between type I and
type II morphs from the Ivindo River (Fig.
1; Table 1). By
contrast, when randomly selected male EODs of one of these morphs are compared
to phase-altered male EODs of the other morph (e.g.
Fig. 10B, right column), phase
shift angles of 45-145° tend to yield the best fit between waveforms
(Fig. 10C, right plot). While
most values of that minimize the total squared deviation between
waveforms are centered around 60° and 120°, some fall close to 90°
(Fig. 10D). Applied to female
EODs of Brienomyrus sp. `VAD', phase shift angles in this same range
maximally inhibited evoked courtship rasps during playbacks to males on their
well-spaced territories in the extreme headwaters of an Ivindo River tributary
(Hopkins and Bass, 1981).
Thus, EOD divergence between males of the two magnostipes-complex
morphs from the Ivindo River appears to be designed for distinctiveness in the
time domain, while simultaneously requiring no change in Knollenorgan
tuning.
Coding of EODs by the Knollenorgan pathway is thought to involve a
comparison of the timing of receptor spikes in opposite body regions (e.g.
head versus tail or right versus left), which respond to
oppositely directed transients in the same EOD (i.e. positive going or
negative going) due to the different directions of current flow with respect
to the inside of the animal (Amagai,
1998; Amagai et al.,
1998; Friedman and Hopkins,
1998). In the simplest version of this model, midbrain analysis of
latencies between two spikes generated by Knollenorgans in opposing body
regions mediates estimation of EOD duration
(Hopkins and Bass, 1981). In
the present study, we show that EODs produced by either the type II or type
III morph elicit patterns of Knollenorgan spiking that are more complex than a
simple two-spike response. EODs of other Brienomyrus species from
Gabon are also known to be coded at the periphery by relatively complex
patterns of Knollenorgan spiking [see Hopkins, p. 567
(Hopkins, 1986)].
Excluding the focal morphs, whose status as biological species remains
uncertain, 10 other species of Gabon-clade Brienomyrus occur at the
most species-rich locality known for this group: Loa-Loa Rapids
(Arnegard et al., 2005). Any
Brienomyrus species (or morph) is likely to experience differing
levels of aggressive threat, niche overlap or reproductive competition from
the other species (and morphs) with which it co-occurs. To the extent that
this holds true, recognition of numerous kinds of EOD waveforms is expected to
be adaptive. A locus for such recognition would require integration of
multiple latencies between spikes generated by populations of Knollenorgans
residing in opposite body regions. A candidate site for this integration is
nucleus exterolateralis pars posterior (ELp)
(Haugedé-Carré,
1979; Amagai, 1998;
Friedman and Hopkins, 1998).
However, because Knollenorgan responses to EODs vary predictably with
orientation of a sender and its distance from the receiver, recognition may
involve other sensory modalities providing information on sender position
(Moller, 2002). Alternate loci
for EOD template matching, if it occurs, are the higher centers that receive
input from ELp as well as other sensory systems (see
Xu-Friedman and Hopkins,
1999).
Wave-type gymnotiform and mormyriform fish are sensitive to temporal
disparities between signals from different body regions in the microsecond to
sub-microsecond range (Carr et al.,
1986; Kawasaki and Guo,
1996). `Dear enemy' recognition of conspecifics based on very
slight differences in EOD waveforms is known from laboratory studies with
pulse-type species in both taxonomic groups
(McGregor and Westby, 1992;
Hanika and Kramer, 2005).
Using a conditioned discrimination task, Paintner and Kramer recently
demonstrated that the mormyrid, Pollimyrus adspersus, can distinguish
EODs varying only in phase spectra
(Paintner and Kramer, 2003).
Why, then, did we only find moderate evidence for discrimination of large
temporal differences in EOD waveforms?
Our design for the first playback study aimed at this system was based on
an expectation that breeding males would preferentially respond to homotypic
EODs, at least when they were paired against heterospecific EODs of a
reproductively isolated, sympatric species. We reasoned that homotypic EODs
would serve as `marker traits' (e.g.
Bolnick and Doebeli, 2003) for
the presence of reproductive competitors or fitness-enhancing spawning
opportunities. In general, a functional role for EODs as species markers is
suggested by patterns of sympatric waveform variation among other members of
Gabon's Brienomyrus species flock. However, statistically significant
support for our expectation was only found for one of two correlated responses
by type I (i.e. rate of burst production) and type II (i.e. proximity) when
homotypic EODs were presented together with those of `CAB'. Social isolation
may have partially masked the EOD preferences we expected to find. Mormyrids
are known to respond to a variety of electrical playbacks, including
artificial stimuli such as brief square waves
(Kramer, 1990;
Moller, 1995). Type I and type
II males almost invariably responded vigorously to both paired signals during
any playback trial. Confining males in playback chambers may have exaggerated
a novelty response in these subjects to any EOD stimulus at all.
When female EODs of alternate magnostipes-complex morphs were
played as pairs, only type II males exhibited preferential responses to
homotypic EODs. Because we have not directly observed spawning by morphs of
the magnostipes complex, we have no knowledge of SPI patterns during
courtship sequences in this group (cf.
Hopkins and Bass, 1981;
Carlson and Hopkins, 2004).
Therefore, we caution that the observed asymmetry in response between morphs
should not currently be interpreted as an actual asymmetry in male mating
preference. In addition to the stress of social isolation and/or any genuine
male mating preferences that may be present, outcomes of our playback
experiments could have been influenced by male-male interactions such as
aggression and territoriality (Maan et
al., 2004; Dijkstra et al.,
2006). Although we presented female-like EODs to isolated males
soon after capture, responses exhibited by both type I and type II males
included head butting and biting directed at the electrodes
(Bell et al., 1974;
Hanika and Kramer, 2005).
Males also responded to playbacks by producing short bursts of EODs, often
preceding them with brief cessations of electromotor output. Such displays are
associated with overt aggression in a wide variety of mormyrid species
(Kramer, 1979;
Hopkins, 1986;
Moller, 1995;
Carlson, 2002).
Outcomes of agonistic encounters are strongly influenced by relative body
size in many animals (Leimar et al.,
1991; Hughes,
1996; Calsbeek and Sinervo,
2002; Lindström and
Pampoulie, 2004), including mormyrids
(Bell et al., 1974). Besides
the anatomical correlates of EOD variation (e.g.
Bass, 1986), body size is
currently the only phenotypic character known to be associated with parallel
cases of sympatric EOD divergence in the magnostipes complex. In the
Ivindo River, breeding males of the type I morph are significantly larger than
breeding males of the type II morph. Gravid females exhibit a trend in the
same direction.
A statistically significant difference between the responses of type I and type II males to homotypic versus heterotypic EODs is consistent with an asymmetry in aggressive threat posed by the sympatric morphs. Type II males discriminated EODs and responded more vigorously to homotypic signals. Type I males failed to show differential responses to type I versus type II EODs. Based on the extreme genetic similarity of sympatric morphs, it is reasonable to hypothesize that electric organ discharge discrimination was masked in type I males. In the absence of other cues, EODs may provide insufficient information for reliable sex recognition within morphs because some adult males without elongated EODs can be found during the breeding season. With paired presentation of homotypic and heterotypic EODs, a novelty response to type I EODs (even though female-like in waveform) may have been suppressed in type II males due to a risk of aggression from the larger morph. By contrast, type I males may have been less inhibited from responding to novel signals of any waveform, potentially masking their discrimination of EODs in our experimental paradigm.
Beyond the stress of social isolation, other limitations of our study
design likely affected our results. Mormyrids often interact in complex ways
in terms of temporal patterns of electric organ discharge
(Arnegard and Carlson, 2005).
Lack of reciprocal SPI interactions during the playbacks probably heightened
aggression, which males may have expressed concurrently with their mating
preferences. It is also possible that a lack of sensory (e.g. tactile) cues
regarding orientation of the fictive animal's head relative to the model
electric organ (i.e. the playback bipole) contributed noise to our results.
Use of model fish containing embedded electrodes should be considered in
future playback experiments. Despite these limitations, our study has still
yielded important initial indications that EOD diversification between
sympatric morphs functions in communication. Different classes of
magnostipes-complex EODs are precisely encoded at the periphery, and
at least some members of this complex exhibit an ability to behaviorally
discriminate these electrical displays. In the Makokou region, type II males
appear more likely to orient toward, and respond electrically to, female-like
EODs of their own morph than to those of type I. Furthermore, the morphs are
now known to differ behaviorally in their asymmetric responses to homotypic
versus heterotypic EODs in the absence of all other sensory cues.
Consistent with the way in which stabilizing selection for species
recognition affects signal design, EODs of adult females in several mormyrid
assemblages are known for their interspecific variation and intraspecific
stereotypy (Hopkins, 1999;
Arnegard and Hopkins, 2003;
Feulner et al., 2006). Despite
the genetic similarity of co-occurring morphs of the magnostipes
complex (Sullivan et al.,
2002; Sullivan et al.,
2004; Arnegard et al.,
2005), the hypothesis that these forms are associated with an
early stage of sympatric speciation in one or more populations warrants
additional consideration due to this general pattern of EOD variation.
Empirical results and theory suggest that divergence in traits such as body
shape and size, resource use behaviors and/or microhabitat selection can
accompany sympatric speciation under frequency-dependent ecological selection
(Wood and Foote, 1996;
Kondrashov and Kondrashov,
1999; Schliewen et al.,
2001; Doebeli and Dieckmann,
2003; Barluenga et al.,
2006). Male-male competition for access to females and perhaps
other territorial resources may also influence signal divergence and sympatric
lineage branching in important ways
(Seehausen and Schluter, 2004;
Dijkstra et al., 2005;
Dijkstra et al., 2006).
Nevertheless, the previous genetic data suggest that speciation has not
occurred between the sympatric morphs
(Arnegard et al., 2005).
Instead, magnostipes-complex EODs may signal alternate behavioral or
life history strategies (Roff,
2001). If so, geographic variation in the relative abundances of
sympatric morphs may be due to influences of environmental and community
heterogeneity on either the expression of a conditional strategy or the
evolutionarily optimal frequencies of alternate fixed strategies (e.g.
Svensson and Sinervo, 2004).
The above possibilities are not exhaustive, nor are they mutually exclusive
(West-Eberhard, 2003).
Based on our playbacks to isolated males of the magnostipes
complex, EODs of this group appear to function in morph-specific advertisement
and recognition. Improved playback designs targeting conditioned responses or
employing more natural contexts for social groups of test subjects are needed
to better understand the behavioral roles of EOD variation in the
magnostipes complex. Knowledge of female mating preferences is also
critically important to achieving this goal. In addition to initial evidence
of a communication function for waveform variation, the existence of EOD
dimorphisms in several, genetically isolated populations suggests that a
deterministic mechanism (e.g. natural selection) is maintaining discrete
signal variation or driving divergence along EOD lines
(Schluter and Nagel, 1995).
Unless population sizes are extremely large, it would be unlikely to find
signal dimorphisms persisting in several isolated populations simultaneously
if EOD waveform variation were selectively neutral. This pattern of multiple
signal dimorphisms in the magnostipes complex informs us that EOD
diversification can either precede mormyrid lineage splitting or play an
active role early in the speciation process, arising long before genome-wide
genetic differences accumulate between sister species. Our finding of a size
difference between co-occurring morphs provides an important framework for
future experimental studies of the causes and consequences of EOD variation in
this intriguing group of electric fishes.
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Acknowledgments |
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References |
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