Ontogeny of the electric organ discharge and the electric organ in the weakly electric pulse fish Brachyhypopomus pinnicaudatus (Hypopomidae, Gymnotiformes)

I recorded the electric organ discharges (EODs) of 331 immature Brachyhypopomus pinnicaudatus 6–88 mm long. Larvae produced head-positive pulses 1.3 ms long at 7 mm (6 days) and added a second, small head-negative phase at 12 mm. Both phases shortened duration and increased amplitude during growth. Relative to the whole EOD, the negative phase increased duration until 22 mm and amplitude until 37 mm. Fish above 37 mm produced a “symmetric” EOD like that of adult females. I stained cleared fish with Sudan black, or fluorescently labeled serial sections with anti-desmin (electric organ) or anti-myosin (muscle). From day 6 onward, a single electric organ was found at the ventral margin of the hypaxial muscle. Electrocytes were initially cylindrical, overlapping, and stalk-less, but later shortened along the rostrocaudal axis, separated into rows, and formed caudal stalks. This differentiation started in the posterior electric organ in 12-mm fish and was complete in the anterior region of fish with “symmetric” EODs. The lack of a distinct “larval” electric organ in this pulse-type species weakens the hypothesis that all gymnotiforms develop both a temporary (larval) and a permanent (adult) electric organ. Accepted: 1 March 1997     

Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus I. Quantification of day-night changes

The electric organ discharge of the gymnotiform fish Brachyhypopomus pinnicaudatus is a biphasic waveform. The female's electric organ discharge is nearly symmetric but males produce a longer second phase than first phase. In this study, infrared-sensitive video cameras monitored the position of unrestrained fish, facilitating precise measurement of electric organ discharge duration and amplitude every 2 h for 24 h. Males (n=27) increased electric organ discharge duration by 37 ± 12% and amplitude by 24 ± 9% at night and decreased it during the day. In contrast, females (n=8) exhibited only minor electric organ discharge variation over time. Most of a male's increase occurred rapidly within the first 2–3 h of darkness. Electric organ discharge values gradually diminished during the second half of the dark period and into the next morning. Modulation of the second phase of the biphasic electric organ discharge produced most of the duration change in males, but both phases changed amplitude by similar amounts. Turning the lights off at mid-day triggered an immediate increase in electric organ discharge, suggesting modification of existing ion channels in the electric organ, rather than altered genomic expression. Exaggeration of electric organ discharge sex differences implies a social function. Daily reduction of duration and amplitude may reduce predation risk or energy expenditure. Accepted: 12 September 1998     

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

Serotonin (5-HT) is an indirect modulator of the electric organ discharge (EOD) in the weakly electric gymnotiform fish, Brachyhypopomus pinnicaudatus. Injections of 5-HT enhance EOD waveform "masculinity", increasing both waveform amplitude and the duration of the second phase. This study investigated the pharmacological identity of 5-HT receptors that regulate the electric waveform and their effects on EOD amplitude and duration. We present evidence that two sets of serotonin receptors modulate the EOD in opposite directions. We found that the 5HT1AR agonist 8-OH-DPAT diminishes EOD duration and amplitude while the 5HT1AR antagonist WAY100635 increases these parameters. In contrast, the 5HT2R agonist alpha-Me-5-HT increases EOD amplitude but not duration, yet 5-HT-induced increases in EOD duration can be inhibited by blocking 5HT2A/2C-like receptors with ketanserin. These results show that 5-HT exerts bi-directional control of EOD modulations in B. pinnicaudatus via action at receptors similar to mammalian 5HT1A and 5HT2 receptors. The discordant amplitude and duration response suggests separate mechanisms for modulating these waveform parameters.     

Testosterone and 11-ketotestosterone have different regulatory effects on electric communication signals of male Brachyhypopomus gauderio

The communication signals of electric fish can be dynamic, varying between the sexes on a circadian rhythm and in response to social and environmental cues. In the gymnotiform fish Brachyhypopomus gauderio waveform shape of the electric organ discharge (EOD) is regulated by steroid and peptide hormones. Furthermore, EOD amplitude and duration change on different timescales and in response to different social stimuli, suggesting that they are regulated by different mechanisms. Little is known about how androgen and peptide hormone systems interact to regulate signal waveform. We investigated the relationship between the androgens testosterone (T) and 11-ketotestosterone (11-KT), the melanocortin peptide hormone α-MSH, and their roles in regulating EOD waveform of male B. gauderio. Males were implanted with androgen (T, 11-KT, or blank), and injected with α-MSH before and at the peak of androgen effect. We compared the effects of androgen implants and social interactions by giving males a size-matched male stimulus with which they could interact electrically. Social stimuli and both androgens increased EOD duration, but only social stimuli and 11-KT elevated amplitude. However, no androgen enhanced EOD amplitude to the extent of a social stimulus, suggesting that a yet unidentified hormonal pathway regulates this signal parameter. Additionally, both androgens increased response of EOD duration to α-MSH, but only 11-KT increased response of EOD amplitude to α-MSH. Social stimuli had no effect on EOD response to α-MSH. The finding that EOD amplitude is preferentially regulated by 11-KT in B. gauderio may provide the basis for independent control of amplitude and duration.     

Variation of electric organ discharge in Mormyrus kannume (Mormyridae) from south-western Ethiopia in relation to individual size,sex and reproductive status

Five variables of the electric organ discharge (EOD) were studied in 132 freshly caught individuals of Mormyrus kannume from the Gibe and Gojeb rivers (the enclosed Omo-Turkana system) and Baro River (the White Nile system) in south-western Ethiopia, East Africa. Most individuals exhibited the typical biphasic EODs with an initial head-positive phase followed by a head-negative phase exceeding initial one in the relative amplitude. In three repeated samples from the Gibe, stable differences in the discharge variables between females and males were found, while no sex differences were observed in other samples. In three cases, a positive correlation between the individual size and discharge duration was found: in two male subsamples from the Gibe and in a mixed sample of both sexes from the Gojeb. In most samples studied, some males exhibited the outstandingly long EOD duration. At the same time, no relationships between the discharge variables and reproductive status of individuals were found. The possible influence of individual and intra-individual variations on the results of inter-population and interspecific comparisons of the discharge variables in mormyrids are highlighted.     

Ontogenetic development of electric-organ discharges in a mormyrid fish, the bulldog Marcusenius macrolepidotus (South African form)

The emergence and development of the electric-organ discharge (EOD) in larvae and juvenile bulldog Marcusenius macrolepidotus was investigated. Larvae hatched 4–5 days after spawning, and the first EODs were recorded on days 9 and 10 at a standard length ( L _S) of c. 6·5 mm. The larval EOD waveform was virtually monopolar, with a strong head-positive phase followed by a weak head-negative phase of long duration. A small separate potential preceded the EOD by c. 1·6 ms (believed to represent postsynaptic potential from electrocyte stalks). In contrast to previous reports on Pollimyrus adspersus with its distinct larval and adult EODs, in M. macrolepidotus there was a gradual transformation of the larval into the adult EOD waveform. The transformation started at an L _S of c. 17 mm (at an age of c. 40 days), first indications being a decrease in duration of the head-negative phase, and an increase of its peak amplitude relative to that of the head-positive phase. Still later, the weak postpotential of the adult EOD emerged on the rising edge of the head-negative phase. The transformation was nearly completed at an L _S of c. 30 mm (at an age of c. 60 days). Evolutionary and behavioural consequences of this alternative path of EOD ontogeny are discussed.     

Melanocortins regulate the electric waveforms of gymnotiform electric fish

The hypothalamic-pituitary-adrenal/interrenal axis couples serotonergic activity in the brain to the peripheral regulators of energy balance and response to stress. The regulation of peripheral systems occurs largely through the release of peptide hormones, especially the melanocortins (adrenocorticotropic hormone [ACTH] and alpha melanocyte stimulating hormone [α-MSH]), and beta-endorphin. Once in circulation, these peptides regulate a wide range of processes; α-MSH in particular regulates behaviors and physiologies with sexual and social functions. We investigated the role of the HPI and melanocortin peptides in regulation of electric social signals in the gymnotiform electric fish, Brachyhypopomus pinnicaudatus. We found that corticotropin releasing factor, thyrotropin-releasing hormone, and α-MSH, three peptide hormones of the HPI/HPA, increased electric signal waveform amplitude and duration when injected into free-swimming fish. A fourth peptide, a synthetic cyclic-α-MSH analog attenuated the normal circadian and socially-induced EOD enhancements in vivo. When applied to the electrogenic cells (electrocytes) in vitro, only α-MSH increased the amplitude and duration of the electrocyte discharge similar to the waveform enhancements seen in vivo. The cyclic-α-MSH analog had no effect on its own, but blocked or attenuated α-MSH-induced enhancements in the single-cell discharge parameters, demonstrating that this compound functions as a silent antagonist at the electrocyte. Overall, these results strongly suggest that the HPI regulates the EOD communication signal, and demonstrate that circulating melanocortin peptides enhance the electrocyte discharge waveform.     

Ontogeny and evolution of electric organs in gymnotiform fish

In order to further our understanding of the evolution of electric organs in the Neotropical gymnotiform fish, we studied the ontogeny of the electric organs in eight species. In Eigenmannia virescens, Sternopygus macrurus, and Apteronotus leptorhynchus the earliest electrocytes are located between muscle fibres of the hypaxial muscle (Type A electrocytes). We present arguments that these Type A electrocytes represent the plesiomorphic condition. In S. macrurus, in addition to the electrocytes in the hypaxial muscle, additional electrocytes were found in the epaxial muscle. In A. leptorhynchus a neurogenic organ develops later during ontogeny in the medial part of the hypaxial muscle in addition to the early myogenic organ. In E. virescens the early electrocytes in hypaxial muscle will degenerate later during ontogeny, and this organ will be replaced functionally by electrocytes located in the caudal appendage and below the hypaxial muscle. In Electrophorus electricus, two Gymnotus species, Rhamphichthys sp., and Brachyhypopomus pinnicaudatus the first electrocytes were found below the hypaxial muscle (Type B electrocytes); they are assumed to be the more derived stage. In R. sp., and B. pinnicaudatus the electrocytes of Type B developed directly into the adult organ. In the two Gymnotus ssp. electrocytes were also found in the medial part of the organ in-between muscle fibres of the hypaxial muscle. In E. electricus a germinative zone was observed to separate from the ventral myotome. This zone is generating electrocytes continuously so that, as a consequence, the relative proportion of electric organ to muscle increases greatly. In 45 mm long E. electricus a separation of low voltage orientation pulses and high voltage trains of pulses (shocks) was observed. A first appearance of Hunter’s organ was found in 140 mm specimens of E. electricus. The first discharges of all species studied were head- positive, with the exception of R. sp., which produced a triphasic discharge, its main component, however, being head-positive. The arguments presented indicate that the Type A electrocytes found in E. virescens, S. macrurus, and A. leptorhynchus would represent the plesiomorphic condition. On the basis of the evidence regarding the formation, cytological appearance, and anatomical location, as well as the early electrical recordings, we would hypothesise that during the evolution of gymnotiforms wave type species evolved first, and in a second step pulse type species followed. This view, however, is corroborated by only some phylogenetic hypotheses.     

Androgen modulates the kinetics of the delayed rectifying K+ current in the electric organ of a weakly electric fish

Weakly electric fish such as Sternopygus macrurus utilize a unique signal production system, the electric organ (EO), to navigate within their environment and to communicate with conspecifics. The electric organ discharge (EOD) generated by the Sternopygus electric organ is quasi-sinusoidal and sexually dimorphic; sexually mature males produce long duration EOD pulses at low frequencies, whereas mature females produce short duration EOD pulses at high frequencies. EOD frequency is set by a medullary pacemaker nucleus, while EOD pulse duration is determined by the kinetics of Na+ and K+ currents in the electric organ. The inactivation of the Na+ current and the activation of the delayed rectifying K+ current of the electric organ covary with EOD frequency such that the kinetics of both currents are faster in fish with high (female) EOD frequency than those with low (male) EOD frequencies. Dihydrotestosterone (DHT) implants masculinize the EOD centrally by decreasing frequency at the pacemaker nucleus (PMN). DHT also acts at the electric organ, broadening the EO pulse, which is at least partly due to a slowing of the inactivation kinetics of the Na+ current. Here, we show that chronic DHT treatment also slows the activation and deactivation kinetics of the electric organ's delayed rectifying K+ current. Thus, androgens coregulate the time-varying kinetics of two distinct ion currents in the EO to shape a sexually dimorphic communication signal.     

Spatial distribution of the medullary command signal within the electric organ of Gymnotus carapo

The pacemaker nucleus of Gymnotus carapo contains two types of neurons: pacemaker cells which set up the frequency of the electric organ discharge (EOD) and relay cells which convey the command signal to the spinal cord. Direct activation of a single relay cell provides enough excitation to discharge a pool of spinal electromotor neurons and electrocytes, generating a small EOD (unit EOD). Different relay cells generate unit EODs of variable size and waveform, indicating the involvement of different groups of electrocytes. A special technique of EOD recording (multiple air-gap) was combined with intracellular stimulation of relay cells to study the spatial distribution within the electric organ (EO) of the command signal arising from different relay cells. Three types of relay cells could be identified: type I commanding the rostral 10% of the EO, type II which distribute their command all along the EO and type III driving the caudal 30%. Waveform analysis of unit EODs indicates that doubly innervated electrocytes which are the most relevant for attaining the specific EOD waveform, receive a favored command from the pacemaker nucleus.Abbreviations CV conduction velocity - EMF electromotive force - EMN electromotor neuron - EO electric organ - EOD electric organ discharge - PN pacemaker nucleus - uEOD unit electric organ discharge     

Phase and amplitude maps of the electric organ discharge of the weakly electric fish,Apteronotus leptorhynchus

Summary The electric organ discharge (EOD) potential was mapped on the skin and midplane of several Apteronotus leptorhynchus. The frequency components of the EOD on the surface of the fish have extremely stable amplitude and phase. However, the waveform varies considerably with different positions on the body surface. Peaks and zero crossings of the potential propagate along the fish's body, and there is no point where the potential is always zero. The EOD differs significantly from a sinusoid over at least one third of the body and tail. A qualitative comparison between fish showed that each individual had a unique spatiotemporal pattern of the EOD potential on its body.The potential waveforms have been assembled into high temporal and spatial resolution maps which show the dynamics of the EOD. Animation sequences and Macintosh software are available by anonymous ftp (mordor.cns.caltech.edu; cd/pub/ElectricFish).We interpret the EOD maps in terms of ramifications on electric organ control and electroreception. The electrocytes comprising the electric organ do not all fire in unison, indicating that the command pathway is not synchronized overall. The maps suggest that electroreceptors in different regions fulfill different computational roles in electroreception. Receptor mechanisms may exist to make use of the phase information or harmonic content of the EOD, so that both spatial and temporal patterns could contribute information useful for electrolocation and communication.Abbreviations EOD electric organ discharge - EO electric organ - CV coefficient of variance     

Environmental and hormonal influences upon EOD waveform in gymnotiform pulse fish.

Temperature is a major variable that affects all biological systems. Environmental temperature determines animal geographical distribution and activity, and influences their reproductive cycle, particularly within the temperate zone. Temperature, as a physical parameter, also strongly affects excitable tissues. The hypothesis of temperature as the most important environmental cue for the onset of breeding in gymnotiform pulse fish of the temperate zone is supported by: (a) a clear temporal correlation that was observed in the wild between water temperature and sexual maturity, and (b) the induction of gonadal maturation and sexual differences after acclimation at high temperature (28 degrees C) in the laboratory. Temperature sensitivity of EOD waveform (described in Brachyhypopomus pinnicaudatus and Gymnotus carapo) is characterized by the decrease of the EOD's late head-negative phase as temperature increases. This phenomenon depends on electrocyte properties since: (a) experimentally induced changes of discharge rate at constant temperature generate smaller EOD distortion, and (b) the effect of temperature upon EOD also depends on water conductivity. Temperature sensitivity of EOD waveform is negatively correlated with gonadal maturity in Brachyhypopomus pinnicaudatus. High temperature sensitivity was observed during the non-breeding season, whereas low temperature sensitivity was recorded during the breeding season. Temperature sensitivity of EOD waveform in both Brachyhypopomus pinnicaudatus and Gymnotus carapo was modulated by: (a) testosterone treatment (100 microg/g) that decreased temperature sensitivity, and (b) acclimation at high temperature (28 degrees C, 1 month) that also decreased temperature sensitivity. Temperature is probably acting through the neuroendocrine system, and ultimately interacting with steroid hormones in their effects upon EOD waveform.     

Temperature sensitivity of the electric organ discharge waveform in Gymnotus carapo

At the southern boundary of gymnotiform distribution in America. water temperature changes seasonally, and may be an environmental cue for the onset of breeding. In this study, we aim to describe the role of temperature upon electric organ discharge waveform in Gymnotus carapo, order Gymnotiformes, family Gymnotidae, and to analyze its interactions with the effects of steroid hormones. The effects of water temperature within its natural range were explored using different protocols. All fish tested had temperature-sensitive electric organ discharge waveforms: the amplitude of the last head-negative component (V4) decreased as temperature increased. Rate increases elicited by electrical stimulation had similar but smaller effect on waveform. Temperature sensitivity is a peripheral phenomenon that depends on the conductivity of the aquatic media. We found hormonal-dependent changes in the electric organ discharge waveform not previously described in this species. The amplitude and duration of V4 increased after testosterone administration. Both testosterone treatment and acclimation by sustained temperature at 27-28 degrees C (environmental simulation of breeding conditions) induced a decrease in temperature sensitivity. As in the related species Brachyhypopomus pinnicaudatus, our data strongly suggest interactions between temperature sensitivity of the electric organ discharge waveform and sexual maturity that might be crucial for reproduction.     

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fish Paramormyrops kingsleyae

Communication signals serve crucial survival and reproductive functions. In Gabon, the widely distributed mormyrid fish Paramormyrops kingsleyae emits an electric organ discharge (EOD) signal with a dual role in communication and electrolocation that exhibits remarkable variation: populations of P. kingsleyae have either biphasic or triphasic EODs, a feature that characterizes interspecific signal diversity among the Paramormyrops genus. We quantified variation in EODs of 327 P. kingsleyae from nine populations and compared it to genetic variation estimated from microsatellite loci. We found no correlation between electric signal and genetic distances, suggesting that EOD divergence cannot be explained by drift alone. An alternative hypothesis is that EOD differences are used for mate discrimination, which would require P. kingsleyae be capable of differentiating between divergent EOD waveforms. Using a habituation-dishabituation assay, we found that P. kingsleyae can discriminate between biphasic and triphasic EOD types. Nonetheless, patterns of genetic and electric organ morphology divergence provide evidence for hybridization between these signal types. Although reproductive isolation with respect to signal type is incomplete, our results suggest that EOD variation in P. kingsleyae could be a cue for assortative mating.     

Electric organ morphology of Sternopygus macrurus,a wave-type,weakly electric fish with a sexually dimorphic EOD

In several species of electric fish with a sex difference in their pulse-type electric organ discharge (EOD), the action potential-generating cells of the electric organ (electrocytes) of males are larger and more invaginated compared to females. Androgen treatment of females and juveniles produces a longer-duration EOD pulse that mimics the mature male EOD, with a concurrent increase in electrocyte size and/or membrane infolding. In Sternopygus macrurus, which generates a wave-type EOD, androgen also increases EOD pulse duration. To investigate possible morphological correlates of hormone-dependent changes in EOD in Sternopygus, we examined electric organs from both fish collected in the field, and untreated and androgen-treated specimens in the laboratory. The electrocytes are cigar shaped, with prominent papillae on the posterior, innervated end. Electrocytes of field-caught specimens were significantly larger in all parameters than were electrocytes of specimens maintained in the laboratory. EOD pulse duration and frequency were highly correlated, and were significantly different between the sexes in sexually mature fish. Nevertheless, no sex difference in electrocyte morphology was observed, nor did any parameters of electrocyte morphology correlate with EOD pulse duration or frequency. Further, whereas androgen treatment significantly lowered EOD frequency and broadened EOD pulse duration, there was no difference in electrocyte morphology between hormone-treated and control groups. Thus, in contrast to results from studies on both mormyrid and gymnotiform pulse fish, electrocyte morphology is not correlated with EOD waveform characteristics in the gymnotiform wave-type fish Sternopygus. The data, therefore, suggest that sex differences in EOD are dependent on changes in active electrical properties of electrocyte membranes. © 1992 John Wiley & Sons, Inc.     

Behavioral detection of electric signal waveform distortion in the weakly electric fish,Gnathonemus petersii

The novelty response of weakly electric mormyrids is a transient acceleration of the rate of electric organ discharges (EOD) elicited by a change in stimulus input. In this study, we used it as a tool to test whether Gnathonemus petersii can perceive minute waveform distortions of its EOD that are caused by capacitive objects, as would occur during electrolocation. Four predictions of a hypothesis concerning the mechanism of capacitance detection were tested and confirmed: (1) G. petersii exhibited a strong novelty response to computer-generated (synthetic) electric stimuli that mimic both the waveform and frequency shifts of the EOD caused by natural capacitive objects (Fig. 3). (2) Similar responses were elicited by synthetic stimuli in which only the waveform distortion due to phase shifting the EOD frequency components was present (Fig. 4). (3) Novelty responses could reliably be evoked by a constant amplitude phase shifted EOD that effects the entire body of the fish evenly, i.e., a phase difference across the body surface was lacking (Figs. 3, 4). (4) Local presentation of a phase-shifted EOD mimic that stimulated only a small number of electroreceptor organs at a single location was also effective in eliciting a behavioral response (Fig. 5).Our results indicate that waveform distortions due to phase shifts alone, i.e. independent of amplitude or frequency cues, are sufficient for the detection of capacitive, animate objects. Mormyrids perceive even minute waveform changes of their own EODs by centrally comparing the input of the two types of receptor cells within a single mormyromast electroreceptor organ. Thus, no comparison of differentially affected body regions is necessary. This shows that G. petersii indeed uses a unique mechanism for signal analysis, which is different from the one employed by gymnotiform wavefish.Abbreviations EOD electric organ discharge - p-p-amplitude peak-to-peak amplitude     

Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation

Weakly electric fish can detect nearby objects and analyse their electric properties during active electrolocation. Four individuals of the South American gymnotiform fish Eigenmannia sp., which emits a continuous wave-type electric signal, were tested for their ability to detect capacitive properties of objects and discriminate them from resistive properties. For individual fish, capacitive values of objects had to be greater than 0.22–1.7 nF (`lower threshold') and smaller than 120–680 nF (`upper threshold') in order to be detected. The capacitive values of natural objects fall well within this detection range. All fish trained could discriminate unequivocally between capacitive and resistive object properties. Thus, fish perceive capacitive properties as a separate object quality. The effects of different types of objects on the locally occurring electric signals which stimulate electroreceptors during electrolocation were examined. Purely resistive objects altered mainly local electric organ discharge (EOD) amplitude, but capacitive objects with values between about 0.5 and 600 nF changed the timing of certain EOD parameters (phase-shift) and EOD waveform. A mechanism for capacitance detection in wave-type electric fish based on time measurements is proposed and compared with the capacitance detection mechanism in mormyrid pulse-type fish, which is based on waveform measurements. Accepted: 31 July 1997     

Mate preference in female electric fish, Brachyhypopomus pinnicaudatus

Weakly electric fish communicate with brief electrostatic field pulses called electric organ discharges (EODs). EOD waveforms are sexually dimorphic in most genera, a condition thought to result from mate choice acting to shape the electric signal's constituent action potentials. We have no direct behavioural evidence that sexual selection by either mate choice or intrasexual competition is responsible for sex differences in the EOD waveforms of electric fish. We explored sexual selection in electric fish by conducting two-choice unforced preference tests with live, unaltered gymnotiform electric fish,Brachyhypopomus pinnicaudatus , which are sexually dimorphic. In the initial test, gravid females selected males over females only when the males were larger than average. Gravid females in later tests preferred larger males to smaller males in a significant majority of those trials in which they showed a preference. In about one-third of those trials, females spawned with their preferred male, confirming their preference. We concluded that passage through the choice apparatus was related to mate choice. The signals of chosen males had larger EOD amplitudes and longer EOD durations. These findings show that femaleB. pinnicaudatus do have a preference for a certain male phenotype. The system requires additional study to dissociate correlated male phenotypic characters to identify which male traits the female prefers. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatry

Striking trait polymorphisms are worthy of study in natural populations because they can often shed light on processes of phenotypic divergence and specialization, adaptive evolution, and (in some cases) the early stages of speciation. We examined patterns of genetic variation within and between populations of mormyrid fishes that are morphologically cryptic in sympatry but produce alternate types of electric organ discharge (EOD). Other species in a large group containing a clade of these morphologically cryptic EOD types produce stereotyped, species-typical EOD waveforms thought to function in mate recognition. First, for six populations from Gabon's Brienomyrus species flock, we confirm that forms of electric fish that exhibit distinctive morphologies and unique EOD waveforms (i.e., good reference species) are reproductively isolated from coexisting congeners. These sympatric species deviate from genetic panmixia across five microsatellite loci. Given this result, we examined three focal pairs of syntopic and morphologically cryptic EOD waveform types that are notable exceptions to the pattern of robust genetic partitioning among unique waveform classes within assemblages. These exceptional pairs constitute a monophyletic group within the Brienomyrus flock known as the magnostipes complex. One member of each pair (type I) produces a head-negative EOD, while the other member (either type II or type III, depending on location) produces a longer duration EOD differing in waveform from type I. We show that signal development in these pairs begins with juveniles of all magnostipes-complex morphs emitting head-positive EODs resembling those of type II adults. Divergence of EOD waveforms occurs with growth such that there are two discrete and fixed signal types in morphologically indistinguishable adults at each of several localities. Strong microsatellite partitioning between allopatric samples of any of these morphologically cryptic signal types suggests that geographically isolated populations are genetically decoupled from one another. By contrast, sympatric morphs appear genetically identical across microsatellite loci in Mouvanga Creek and the Okano River and only very weakly diverged, if at all, in the Ivindo River. Our results for the magnostipes complex fail to detect species boundaries between the focal morphs and are, instead, fully consistent with the existence of relatively stable signal dimorphisms at each of several different localities. No mechanism for the maintenance of this electrical polymorphism is suggested by the known natural history of the magnostipes complex. Despite a lack of evidence for genetic differentiation, the possibility of incipient sympatric speciation between morphs (especially type I and type II within the Ivindo River) merits further testing due to behavioral and neurobiological lines of evidence implying a general role for stereotyped EOD waveforms in species recognition. We discuss alternative hypotheses concerning the origins, stability, and evolutionary significance of these intriguing electrical morphs in light of geographical patterns of population structure and signal variation.     

Signal variation and its morphological correlates in <Emphasis Type="Italic">Paramormyrops kingsleyae</Emphasis> provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish

We describe patterns of geographic variation in electric signal waveforms among populations of the mormyrid electric fish species Paramormyrops kingsleyae. This analysis includes study of electric organs and electric organ discharge (EOD) signals from 553 specimens collected from 12 localities in Gabon, West-Central Africa from 1998 to 2009. We measured time, slope, and voltage values from nine defined EOD “landmarks” and determined peak spectral frequencies from each waveform; these data were subjected to principal components analysis. The majority of variation in EODs is explained by two factors: the first related to EOD duration, the second related to the magnitude of the weak head-negative pre-potential, P0. Both factors varied clinally across Gabon. EODs are shorter in eastern Gabon and longer in western Gabon. Peak P0 is slightly larger in northern Gabon and smaller in southern Gabon. P0 in the EOD is due to the presence of penetrating-stalked (Pa) electrocytes in the electric organ while absence is due to the presence of non-penetrating stalked electrocytes (NPp). Across Gabon, the majority of P. kingsleyae populations surveyed have only individuals with P0-present EODs and Pa electrocytes. We discovered two geographically distinct populations, isolated from others by barriers to migration, where all individuals have P0-absent EODs with NPp electrocytes. At two sites along a boundary between P0-absent and P0-present populations, P0-absent and P0-present individuals were found in sympatry; specimens collected there had electric organs of intermediate morphology. This pattern of geographic variation in EODs is considered in the context of current phylogenetic work. Multiple independent paedomorphic losses of penetrating stalked electrocytes have occurred within five Paramormyrops species and seven genera of mormyrids. We suggest that this key anatomical feature in EOD signal evolution may be under a simple mechanism of genetic control, and may be easily influenced by selection or drift throughout the evolutionary history of mormyrids.