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The electric organ (EO) of weakly electric mormyrids consists of flat, disk-shaped electrocytes with distinct anterior and posterior faces. There are multiple species-characteristic patterns in the geometry of the electrocytes and their innervation. To further correlate electric organ discharge (EOD) with EO anatomy, we examined four species of the mormyrid genus Campylomormyrus possessing clearly distinct EODs. In C. compressirostris, C. numenius, and C. tshokwe, all of which display biphasic EODs, the posterior face of the electrocytes forms evaginations merging to a stalk system receiving the innervation. In C. tamandua that emits a triphasic EOD, the small stalks of the electrocyte penetrate the electrocyte anteriorly before merging on the anterior side to receive the innervation. Additional differences in electrocyte anatomy among the former three species with the same EO geometry could be associated with further characteristics of their EODs. Furthermore, in C. numenius, ontogenetic changes in EO anatomy correlate with profound changes in the EOD. In the juvenile the anterior face of the electrocyte is smooth, whereas in the adult it exhibits pronounced surface foldings. This anatomical difference, together with disparities in the degree of stalk furcation, probably contributes to the about 12 times longer EOD in the adult.
Voltage-gated sodium channels, Nav1, play a crucial role in the generation and propagation of action potentials and substantially contribute to the shape of their rising phase. The electric organ discharge (EOD) of African weakly electric fish (Mormyroidea) is the sum of action potentials fired from all electrocytes of the electric organ at the same time and hence voltage-gated sodium channels are one factor—together with the electrocyte’s morphology and innervation pattern—that determines the properties of these EODs. Due to the fish-specific genome duplication, teleost fish possess eight copies of sodium channel genes (SCN), which encode for Nav1 channels. In mormyroids, SCN4aa is solely expressed in the electrocytes of the adult electric organ. In this study, we compared entire SCN4aa sequences of six species of the genus Campylomormyrus and identified nonsynonymous substitutions among them. SCN4aa in Campylomormyrus exhibits a much higher evolutionary rate compared to its paralog SCN4ab, whose expression is not restricted to the electric organ. We also found evidence for strong positive selection on the SCN4aa gene within Mormyridae and along the lineage ancestral to the Mormyridae. We have identified sites at which all nonelectric teleosts are monomorphic in their amino acid, but mormyrids have different amino acids. Our findings confirm the crucial role of SCN4aa in EOD evolution among mormyrid weakly electric fish. The inferred positive selection within Mormyridae makes this gene a prime candidate for further investigation of the divergent evolution of pulse-type EODs among closely related species.
The aim of this study was a longitudinal description of the ontogeny of the adult electric organ of Campylomormyrus rhynchophorus which produces as adult an electric organ discharge of very long duration (ca. 25 ms). We could indeed show (for the first time in a mormyrid fish) that the electric organ discharge which is first produced early during ontogeny in 33-mm-long juveniles is much shorter in duration and has a different shape than the electric organ discharge in 15-cm-long adults. The change from this juvenile electric organ discharges into the adult electric organ discharge takes at least a year. The increase in electric organ discharge duration could be causally linked to the development of surface evaginations, papillae, at the rostral face of the electrocyte which are recognizable for the first time in 65-mm-long juveniles and are most prominent at the periphery of the electrocyte.
In mormyrid weakly electric fish, the electric organ discharge (EOD) is used for species recognition, orientation and prey localization. Produced in the muscle-derived adult electric organ, the EOD exhibits a wide diversity across species in both waveform and duration. While certain defining EOD characteristics can be linked to anatomical features of the electric organ, many factors underlying EOD differentiation are yet unknown. Here, we report the differential expression of 13 Kv1 voltage-gated potassium channel genes, two inwardly rectifying potassium channel genes, two previously studied sodium channel genes and an ATPase pump in two sympatric species of the genus Campylomormyrus in both the adult electric organ and skeletal muscle. Campylomormyrus compressirostris displays a basal EOD, largely unchanged during development, while C. tshokwe has an elongated, putatively derived discharge. We report an upregulation in all Kv1 genes in the electric organ of Campylomormyrus tshokwe when compared to both skeletal muscle and C. compressirostris electric organ. This pattern of upregulation in a species with a derived EOD form suggests that voltage-gated potassium channels are potentially involved in the diversification of the EOD signal among mormyrid weakly electric fish.
Communication is key to a wide variety of animal behaviours and multiple modalities are often involved in this exchange of information from sender to receiver. The communication of African weakly electric fish, however, is thought to be predominantly unimodal and is mediated by their electric sense, in which species-specific electric organ discharges (EODs) are generated in a context-dependent and thus variable sequence of pulse intervals (SPI). While the primary function of the electric sense is considered to be electrolocation, both of its components likely carry information regarding identity of the sender. However, a clear understanding of their contribution to species recognition is incomplete. We therefore analysed these two electrocommunication components (EOD waveform and SPI statistics) in two sympatric mormyrid Campylomormyrus species. In a set of five playback conditions, we further investigated which components may drive interspecific recognition and discrimination. While we found that both electrocommunication components are species-specific, the cues necessary for species recognition differ between the two species studied. While the EOD waveform and SPI were both necessary and sufficient for species recognition in C. compressirostris males, C. tamandua males apparently utilize other, non-electric modalities. Mapped onto a recent phylogeny, our results suggest that discrimination by electric cues alone may be an apomorphic trait evolved during a recent radiation in this taxon.
Communication is key to a wide variety of animal behaviours and multiple modalities are often involved in this exchange of information from sender to receiver. The communication of African weakly electric fish, however, is thought to be predominantly unimodal and is mediated by their electric sense, in which species-specific electric organ discharges (EODs) are generated in a context-dependent and thus variable sequence of pulse intervals (SPI). While the primary function of the electric sense is considered to be electrolocation, both of its components likely carry information regarding identity of the sender. However, a clear understanding of their contribution to species recognition is incomplete. We therefore analysed these two electrocommunication components (EOD waveform and SPI statistics) in two sympatric mormyrid Campylomormyrus species. In a set of five playback conditions, we further investigated which components may drive interspecific recognition and discrimination. While we found that both electrocommunication components are species-specific, the cues necessary for species recognition differ between the two species studied. While the EOD waveform and SPI were both necessary and sufficient for species recognition in C. compressirostris males, C. tamandua males apparently utilize other, non-electric modalities. Mapped onto a recent phylogeny, our results suggest that discrimination by electric cues alone may be an apomorphic trait evolved during a recent radiation in this taxon.
Effective communication among sympatric species is often instrumental for behavioural isolation, where the failure to successfully discriminate between potential mates could lead to less fit hybrid offspring. Discrimination between con- and heterospecifics tends to occur more often in the sex that invests more in offspring production, i.e. females, but males may also mediate reproductive isolation. In this study, we show that among two Campylomormyrus Africanweakly electric fish species, males preferentially associate with conspecific females during choice tests using live fish as stimuli, i.e. when all sensory modalities potentially used for communication were present. We then conducted playback experiments to determine whether the species-specific electric organ discharge (EOD) used for electrocommunication serves as the cue for this conspecific association preference. Interestingly, only C. compressirostris males associated significantly more with the conspecific EOD waveform when playback stimuli were provided, while no such association preference was observed in C. tamandua males. Given our results, the EOD appears to serve, in part, as a male-mediated pre-zygotic isolation mechanism among sympatric species. However, the failure of C. tamandua males to discriminate between con- and heterospecific playback discharges suggests that multiple modalities may be necessary for species recognition in some African weakly electric fish species.
Effective communication among sympatric species is often instrumental for behavioural isolation, where the failure to successfully discriminate between potential mates could lead to less fit hybrid offspring. Discrimination between con- and heterospecifics tends to occur more often in the sex that invests more in offspring production, i.e. females, but males may also mediate reproductive isolation. In this study, we show that among two Campylomormyrus Africanweakly electric fish species, males preferentially associate with conspecific females during choice tests using live fish as stimuli, i.e. when all sensory modalities potentially used for communication were present. We then conducted playback experiments to determine whether the species-specific electric organ discharge (EOD) used for electrocommunication serves as the cue for this conspecific association preference. Interestingly, only C. compressirostris males associated significantly more with the conspecific EOD waveform when playback stimuli were provided, while no such association preference was observed in C. tamandua males. Given our results, the EOD appears to serve, in part, as a male-mediated pre-zygotic isolation mechanism among sympatric species. However, the failure of C. tamandua males to discriminate between con- and heterospecific playback discharges suggests that multiple modalities may be necessary for species recognition in some African weakly electric fish species.
Background African weakly-electric fishes of the family Mormyridae are able to produce and perceive weak electric signals (typically less than one volt in amplitude) owing to the presence of a specialized, muscle-derived electric organ (EO) in their tail region. Such electric signals, also known as Electric Organ Discharges (EODs), are used for objects/prey localization, for the identification of conspecifics, and in social and reproductive behaviour. This feature might have promoted the adaptive radiation of this family by acting as an effective pre-zygotic isolation mechanism. Despite the physiological and evolutionary importance of this trait, the investigation of the genetic basis of its function and modification has so far remained limited. In this study, we aim at: i) identifying constitutive differences in terms of gene expression between electric organ and skeletal muscle (SM) in two mormyrid species of the genus Campylomormyrus: C. compressirostris and C. tshokwe, and ii) exploring cross-specific patterns of gene expression within the two tissues among C. compressirostris, C. tshokwe, and the outgroup species Gnathonemus petersii. Results Twelve paired-end (100 bp) strand-specific RNA-seq Illumina libraries were sequenced, producing circa 330 M quality-filtered short read pairs. The obtained reads were assembled de novo into four reference transcriptomes. In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe. Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways. Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome. Conclusions The data obtained indicate that: i) the loss of contractile activity and the decoupling of the excitation-contraction processes are reflected by the down-regulation of the corresponding genes in the electric organ’s transcriptome; ii) the metabolic activity of the EO might be specialized towards the production and turn-over of membrane structures; iii) several ion channels are highly expressed in the EO in order to increase excitability; iv) several myogenic factors might be down-regulated by transcription repressors in the EO.
Background: African weakly-electric fishes of the family Mormyridae are able to produce and perceive weak electric signals (typically less than one volt in amplitude) owing to the presence of a specialized, muscle-derived electric organ (EO) in their tail region. Such electric signals, also known as Electric Organ Discharges (EODs), are used for objects/prey localization, for the identification of conspecifics, and in social and reproductive behaviour. This feature might have promoted the adaptive radiation of this family by acting as an effective pre-zygotic isolation mechanism. Despite the physiological and evolutionary importance of this trait, the investigation of the genetic basis of its function and modification has so far remained limited. In this study, we aim at: i) identifying constitutive differences in terms of gene expression between electric organ and skeletal muscle (SM) in two mormyrid species of the genus Campylomormyrus: C. compressirostris and C. tshokwe, and ii) exploring cross-specific patterns of gene expression within the two tissues among C. compressirostris, C. tshokwe, and the outgroup species Gnathonemus petersii.
Results: Twelve paired-end (100 bp) strand-specific RNA-seq Illumina libraries were sequenced, producing circa 330 M quality-filtered short read pairs. The obtained reads were assembled de novo into four reference transcriptomes. In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C. tshokwe. Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways. Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.
Conclusions: The data obtained indicate that: i) the loss of contractile activity and the decoupling of the excitation-contraction processes are reflected by the down-regulation of the corresponding genes in the electric organ's transcriptome; ii) the metabolic activity of the EO might be specialized towards the production and turn-over of membrane structures; iii) several ion channels are highly expressed in the EO in order to increase excitability; iv) several myogenic factors might be down-regulated by transcription repressors in the EO.