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

ABSTRACT: 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.

SUBMITTER: Picq S

PROVIDER: S-EPMC7816287 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

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

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