Dataset Information

Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish.

ABSTRACT: Mormyrid weakly electric fish produce electric organ discharges (EODs) for active electrolocation and electrocommunication. These pulses are emitted with variable interdischarge intervals (IDIs) resulting in temporal discharge patterns and interactive signaling episodes with nearby conspecifics. However, unequivocal assignment of interactive signaling to a specific behavioral context has proven to be challenging. Using an ethorobotical approach, we confronted single individuals of weakly electric Mormyrus rume proboscirostris with a mobile fish robot capable of interacting both physically, on arbitrary trajectories, as well as electrically, by generating echo responses through playback of species-specific EODs, thus synchronizing signals with the fish. Interactive signaling by the fish was more pronounced in response to a dynamic echo playback generated by the robot than in response to playback of static random IDI sequences. Such synchronizations were particularly strong at a distance corresponding to the outer limit of active electrolocation, and when fish oriented toward the fish replica. We therefore argue that interactive signaling through echoing of a conspecific's EODs provides a simple mechanism by which weakly electric fish can specifically address nearby individuals during electrocommunication. Echoing may thus enable mormyrids to mutually allocate social attention and constitute a foundation for complex social behavior and relatively advanced cognitive abilities in a basal vertebrate lineage.

SUBMITTER: Worm M

PROVIDER: S-EPMC6042124 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish.

Worm Martin M Landgraf Tim T Prume Julia J Nguyen Hai H Kirschbaum Frank F von der Emde Gerhard G

Proceedings of the National Academy of Sciences of the United States of America 20180611 26

Mormyrid weakly electric fish produce electric organ discharges (EODs) for active electrolocation and electrocommunication. These pulses are emitted with variable interdischarge intervals (IDIs) resulting in temporal discharge patterns and interactive signaling episodes with nearby conspecifics. However, unequivocal assignment of interactive signaling to a specific behavioral context has proven to be challenging. Using an ethorobotical approach, we confronted single individuals of weakly electri ...[more]

PMID: 29891707

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Project description:Electric fishes have independently evolved six times. Most of these fish are weakly electric and they use their discharge mainly for orientation and communication. In the African weakly electric fish genus Campylomormyrus, electric organ discharge (EOD) signals are strikingly different in shape and duration among closely related species, they contribute to pre-zygotic isolation and may have triggered an adaptive radiation. We performed mRNA sequencing on electric organs (EOs) and skeletal muscle (SMs; from which the EOs derive) from three species with short (0.4 ms), medium (5 ms), and long (40 ms) EODs and two different cross-species hybrids. Using pairwise comparison of differential gene expression between EOs and SMs, we identified 1,444 up regulated genes in EO shared by all five species/hybrids cohorts, rendering them candidate genes for EO-specific properties in Campylomormyrus. To understand how gene expression contributes to the variation in EOD duration, we made cross species comparisons among species and tissue. We identified three types of EOD-duration-related expression patterns and several candidate genes, including KCNJ2, KLF5 and SLC24a2, their upregulation may contribute to increased EOD duration, along with a down-regulated gene KCNK6. Hybrids between a short (C. compressirostris) and a long (C. rhynchophorus) discharging species exhibit EODs of intermediate duration and showed imbalanced expression of KCNJ2 alleles. The preferential expression of the C. rhynchophorus allele is in line with a higher expression level in that parental species and points towards a cis-regulatory difference at this locus, relative to EOD duration. A further candidate gene, KLF5, is a transcription factor potentially balancing potassium channel gene expression, a crucial process for the formation of an EOD. Unraveling the genetic basis of the species-specific modulation of the EOD in Campylomormyrus is crucial for understanding the adaptive radiation of this emerging model taxon of ecological (perhaps even sympatric) speciation.

Project description:Electric organs (EOs) have evolved independently in vertebrates six times from skeletal muscle (SM). The transcriptional changes accompanying this developmental transformation are not presently well understood. Mormyrids and gymnotiforms are two highly convergent groups of weakly electric fish that have independently evolved EOs: while much is known about development and gene expression in gymnotiforms, very little is known about development and gene expression in mormyrids. This lack of data limits prospects for comparative work. We report here on the characterization of 28 differentially expressed genes between SM and EO tissues in the mormyrid Brienomyrus brachyistius, which were identified using suppressive subtractive hybridization (SSH). Forward and reverse SSH was performed on tissue samples of EO and SM resulting in one cDNA library enriched with mRNAs expressed in EO, and a second library representing mRNAs unique to SM. Nineteen expressed sequence tags (ESTs) were identified in EO and nine were identified in SM using BLAST searching of Danio rerio sequences available in NCBI databases. We confirmed differential expression of all 28 ESTs using RT-PCR. In EO, these ESTs represent four classes of proteins: (1) ion pumps, including the ?- and ?-subunits of Na(+)/K(+)-ATPase, and a plasma membrane Ca(2+)-ATPase; (2) Ca(2+)-binding protein S100, several parvalbumin paralogs, calcyclin-binding protein and neurogranin; (3) sarcomeric proteins troponin I, myosin heavy chain and actin-related protein complex subunit 3 (Arcp3); and (4) the transcription factors enhancer of rudimentary homolog (ERH) and myocyte enhancer factor 2A (MEF2A). Immunohistochemistry and western blotting were used to demonstrate the translation of seven proteins (myosin heavy chain, Na(+)/K(+)-ATPase, plasma membrane Ca(2+)-ATPase, MEF2, troponin and parvalbumin) and their cellular localization in EO and SM. Our findings suggest that mormyrids express several paralogs of muscle-specific genes and the proteins they encode in EOs, unlike gymnotiforms, which may post-transcriptionally repress several sarcomeric proteins. In spite of the similarity in the physiology and function of EOs in mormyrids and gymnotiforms, this study indicates that the mechanisms of development in the two groups may be considerably different.

Project description:Mormyrid weakly electric fish produce short, pulse-type electric organ discharges for actively probing their environment and to communicate with conspecifics. Animals emit sequences of pulse-trains that vary in overall frequency and temporal patterning and can lead to time-locked interactions with the discharge activity of other individuals. Both active electrolocation and electrocommunication are additionally accompanied by stereotypical locomotor patterns. However, the concrete roles of electrical and locomotor patterns during social interactions in mormyrids are not well understood. Here we used a mobile fish dummy that was emitting different types of electrical playback sequences to study following behavior and interaction patterns (electrical and locomotor) between individuals of weakly electric fish. We confronted single individuals of Mormyrus rume proboscirostris with a mobile dummy fish designed to attract fish from a shelter and recruit them into an open area by emitting electrical playbacks of natural discharge sequences. We found that fish were reliably recruited by the mobile dummy if it emitted electrical signals and followed it largely independently of the presented playback patterns. While following the dummy, fish interacted with it spatially by displaying stereotypical motor patterns, as well as electrically, e.g. through discharge regularizations and by synchronizing their own discharge activity to the playback. However, the overall emission frequencies of the dummy were not adopted by the following fish. Instead, social signals based on different temporal patterns were emitted depending on the type of playback. In particular, double pulses were displayed in response to electrical signaling of the dummy and their expression was positively correlated with an animals' rank in the dominance hierarchy. Based on additional analysis of swimming trajectories and stereotypical locomotor behavior patterns, we conclude that the reception and emission of electrical communication signals play a crucial role in mediating social interactions in mormyrid weakly electric fish.

Dataset Information

Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish.

Publications

Evidence for mutual allocation of social attention through interactive signaling in a mormyrid weakly electric fish.

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