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Little is known about the genetic basis of convergent traits that originate repeatedly over broad taxonomic scales. The myogenic electric organ has evolved six times in fishes to produce electric fields used in communication, navigation, predation, or defense. We have examined the genomic basis of the convergent anatomical and physiological origins of these organs by assembling the genome of the electric eel (Electrophorus electricus) and sequencing electric organ and skeletal muscle transcriptomes from three lineages that have independently evolved electric organs. Our results indicate that, despite millions of years of evolution and large differences in the morphology of electric organ cells, independent lineages have leveraged similar transcription factors and developmental and cellular pathways in the evolution of electric organs.

Abstract In the African weakly electric fish genus Campylomormyrus, electric organ discharge signals are strikingly different in shape and duration among closely related species, contribute to prezygotic isolation, and may have triggered an adaptive radiation. We performed mRNA sequencing on electric organs and skeletal muscles (from which the electric organs derive) from 3 species with short (0.4 ms), medium (5 ms), and long (40 ms) electric organ discharges and 2 different cross-species hybrids. We identified 1,444 upregulated genes in electric organ shared by all 5 species/hybrid cohorts, rendering them candidate genes for electric organ–specific properties in Campylomormyrus. We further identified several candidate genes, including KCNJ2 and KLF5, and their upregulation may contribute to increased electric organ discharge duration. Hybrids between a short (Campylomormyrus compressirostris) and a long (Campylomormyrus rhynchophorus) discharging species exhibit electric organ discharges of intermediate duration and showed imbalanced expression of KCNJ2 alleles, pointing toward a cis-regulatory difference at this locus, relative to electric organ discharge duration. KLF5 is a transcription factor potentially balancing potassium channel gene expression, a crucial process for the formation of an electric organ discharge. Unraveling the genetic basis of the species-specific modulation of the electric organ discharge in Campylomormyrus is crucial for understanding the adaptive radiation of this emerging model taxon of ecological (perhaps even sympatric) speciation.

Background Teleost fishes comprise more than half of the vertebrate species. Within teleosts, most phylogenies consider the split between Osteoglossomorpha and Euteleosteomorpha/Otomorpha as basal, preceded only by the derivation of the most primitive group of teleosts, the Elopomorpha. While Osteoglossomorpha are generally species poor, the taxon contains the African weakly electric fish (Mormyroidei), which have radiated into numerous species. Within the mormyrids, the genus Campylomormyrus is mostly endemic to the Congo Basin. Campylomormyrus serves as a model to understand mechanisms of adaptive radiation and ecological speciation, especially with regard to its highly diverse species-specific electric organ discharges (EOD). Currently, there are few well-annotated genomes available for electric fish in general and mormyrids in particular. Our study aims at producing a high-quality genome assembly and to use this to examine genome evolution in relation to other teleosts. This will facilitate further understanding of the evolution of the osteoglossomorpha fish in general and of electric fish in particular. Results A high-quality weakly electric fish ( C. compressirostris ) genome was produced from a single individual with a genome size of 862 Mb, consisting of 1,497 contigs with an N50 of 1,399 kb and a GC-content of 43.69%. Gene predictions identified 34,492 protein-coding genes, which is a higher number than in the two other available Osteoglossomorpha genomes of Paramormyrops kingsleyae and Scleropages formosus . A Computational Analysis of gene Family Evolution (CAFE5) comparing 33 teleost fish genomes suggests an overall faster gene family turnover rate in Osteoglossomorpha than in Otomorpha and Euteleosteomorpha. Moreover, the ratios of expanded/contracted gene family numbers in Osteoglossomorpha are significantly higher than in the other two taxa, except for species that had undergone an additional genome duplication ( Cyprinus carpio and Oncorhynchus mykiss ) . As potassium channel proteins are hypothesized to play a key role in EOD diversity among species, we put a special focus on them, and manually curated 16 Kv1 genes. We identified a tandem duplication in the KCNA7a gene in the genome of C. compressirostris . Conclusions We present the fourth genome of an electric fish and the third well-annotated genome for Osteoglossomorpha, enabling us to compare gene family evolution among major teleost lineages. Osteoglossomorpha appear to exhibit rapid gene family evolution, with more gene family expansions than contractions. The curated Kv1 gene family showed seven gene clusters, which is more than in other analyzed fish genomes outside Osteoglossomorpha. The KCNA7a , encoding for a potassium channel central for EOD production and modulation, is tandemly duplicated which may related to the diverse EOD observed among Campylomormyrus species.

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.

Rivers have long been implicated in the processes of macroevolutionary diversification, but only recently have tools emerged to quantify habitat volume and connectivity across modern and ancient landscapes. Here we compare biodiversity patterns in a diverse clade of Amazonian electric fishes with the predictions of three alternative hypotheses of rivers as: (1) semi-permeable dispersal barriers, (2) branching drainage networks, and (3) dynamic with a reticulated history of connections; i.e., river capture. We found support for all three hypotheses, with large river corridors as partial dispersal barriers to small-river species, interfluves as barriers to large-river species, and contrasting patterns of local (alpha) diversity and species-turnover (beta diversity) in large and small rivers. River captures are faster in smaller rivers with rare but expansive mega-river capture events, facilitating dispersal of small-river clades across watersheds. These results support the role of riverine dynamics as principle agents driving continental diversification of megadiverse tropical aquatic faunas.

African weakly electric fish of the mormyrid genus Campylomormyrus generate pulse-type electric organ discharges (EODs) for orientation and communication. Their pulse durations are species-specific and elongated EODs are a derived trait. So far, differential gene expression among tissue-specific transcriptomes across species with different pulses and point mutations in single ion channel genes indicate a relation of pulse duration and electrocyte geometry/excitability. However, a comprehensive assessment of expressed Single Nucleotide Polymorphisms (SNPs) throughout the entire transcriptome of African weakly electric fish, with the potential to identify further genes influencing EOD duration, is still lacking. This is of particular value, as discharge duration is likely based on multiple cellular mechanisms and various genes. Here we provide the first transcriptome-wide SNP analysis of African weakly electric fish species (genus Campylomormyrus) differing by EOD duration to identify candidate genes and cellular mechanisms potentially involved in the determination of an elongated discharge of C. tshokwe. Non-synonymous substitutions specific to C. tshokwe were found in 27 candidate genes with inferred positive selection among Campylomormyrus species. These candidate genes had mainly functions linked to transcriptional regulation, cell proliferation and cell differentiation. Further, by comparing gene annotations between C. compressirostris (ancestral short EOD) and C. tshokwe (derived elongated EOD), we identified 27 GO terms and 2 KEGG pathway categories for which C. tshokwe significantly more frequently exhibited a species-specific expressed substitution than C. compressirostris. The results indicate that transcriptional regulation as well cell proliferation and differentiation take part in the determination of elongated pulse durations in C. tshokwe. Those cellular processes are pivotal for tissue morphogenesis and might determine the shape of electric organs supporting the observed correlation between electrocyte geometry/tissue structure and discharge duration. The inferred expressed SNPs and their functional implications are a valuable resource for future investigations on EOD durations.

One of the most remarkable examples of convergent evolution among vertebrates is illustrated by the independent origins of an active electric sense in South American and African weakly electric fishes, the Gymnotiformes and Mormyroidea, respectively. These groups independently evolved similar complex systems for object localization and communication via the generation and reception of weak electric fields. While good estimates of divergence times are critical to understanding the temporal context for the evolution and diversification of these two groups, their respective ages have been difficult to estimate due to the absence of an informative fossil record, use of strict molecular clock models in previous studies, and/or incomplete taxonomic sampling. Here, we examine the timing of the origins of the Gymnotiformes and the Mormyroidea using complete mitogenome sequences and a parametric bayesian method for divergence time reconstruction. Under two different fossil-based calibration methods, we estimated similar ages for the independent origins of the Mormyroidea and Gymnotiformes. Our absolute estimates for the origins of these groups either slightly postdate, or just predate, the final separation of Africa and South America by continental drift. The most recent common ancestor of the Mormyroidea and Gymnotiformes was found to be a non-electrogenic basal teleost living more than 85 millions years earlier. For both electric fish lineages, we also estimated similar intervals (16-19 or 22-26 million years, depending on calibration method) between the appearance of electroreception and the origin of myogenic electric organs, providing rough upper estimates for the time periods during which these complex electric organs evolved de novo from skeletal muscle precursors. The fact that the Gymnotiformes and Mormyroidea are of similar age enhances the comparative value of the weakly electric fish system for investigating pathways to evolutionary novelty, as well as the influences of key innovations in communication on the process of species radiation.

Background Understanding the genomic basis of phenotypic diversity can be greatly facilitated by examining adaptive radiations with hypervariable traits. In this study, we focus on a rapidly diverged species group of mormyrid electric fish in the genus Paramormyrops , which are characterized by extensive phenotypic variation in electric organ discharges (EODs). The main components of EOD diversity are waveform duration, complexity and polarity. Using an RNA-sequencing based approach, we sought to identify gene expression correlates for each of these EOD waveform features by comparing 11 specimens of Paramormyrops that exhibit variation in these features. Results Patterns of gene expression among Paramormyrops are highly correlated, and 3274 genes (16%) were differentially expressed. Using our most restrictive criteria, we detected 145–183 differentially expressed genes correlated with each EOD feature, with little overlap between them. The predicted functions of several of these genes are related to extracellular matrix, cation homeostasis, lipid metabolism, and cytoskeletal and sarcomeric proteins. These genes are of significant interest given the known morphological differences between electric organs that underlie differences in the EOD waveform features studied. Conclusions In this study, we identified plausible candidate genes that may contribute to phenotypic differences in EOD waveforms among a rapidly diverged group of mormyrid electric fish. These genes may be important targets of selection in the evolution of species-specific differences in mate-recognition signals.

The ability to generate and detect electric fields has evolved in several groups of fishes as a means of communication, navigation and, occasionally, predation. The energetic burden required can account for up to 20% of electric fishes' daily energy expenditure. Despite this, molecular adaptations that enable electric fishes to meet the metabolic demands of bioelectrogenesis remain unknown. Here, we investigate the molecular evolution of the mitochondrial oxidative phosphorylation (OXPHOS) complexes in the two most diverse clades of weakly electric fishes—South American Gymnotiformes and African Mormyroidea, using codon-based likelihood approaches. Our analyses reveal that although mitochondrial OXPHOS genes are generally subject to strong purifying selection, this constraint is significantly reduced in electric compared to non-electric fishes, particularly for complexes IV and V. Moreover, analyses of concatenated mitochondrial genes show strong evidence for positive selection in complex I genes on the two branches associated with the independent evolutionary origins of electrogenesis. These results suggest that adaptive evolution of proton translocation in the OXPHOS cellular machinery may be associated with the evolution of bioelectrogenesis. Overall, we find striking evidence for remarkably similar effects of electrogenesis on the molecular evolution of mitochondrial OXPHOS genes in two independently derived clades of electrogenic fishes. This article is part of the theme issue ‘Linking the mitochondrial genotype to phenotype: a complex endeavour’.

Most weakly electric fish navigate and communicate by sensing electric signals generated by their muscle-derived electric organs. Adults of one lineage (Apteronotidae), which discharge their electric organs in excess of 1 kHz, instead have an electric organ derived from the axons of specialized spinal neurons (electromotorneurons [EMNs]). EMNs fire spontaneously and are the fastest-firing neurons known. This biophysically extreme phenotype depends upon a persistent sodium current, the molecular underpinnings of which remain unknown. We show that a skeletal muscle-specific sodium channel gene duplicated in this lineage and, within approximately 2 million years, began expressing in the spinal cord, a novel site of expression for this isoform. Concurrently, amino acid replacements that cause a persistent sodium current accumulated in the regions of the channel underlying inactivation. Therefore, a novel adaptation allowing extreme neuronal firing arose from the duplication, change in expression, and rapid sequence evolution of a muscle-expressing sodium channel gene.