Unexpected species diversity in electric eels with a description of the strongest living bioelectricity generator

Is there only one electric eel species? For two and a half centuries since its description by Linnaeus, Electrophorus electricus has captivated humankind by its capacity to generate strong electric discharges. Despite the importance of Electrophorus in multiple fields of science, the possibility of additional species-level diversity in the genus, which could also reveal a hidden variety of substances and bioelectrogenic functions, has hitherto not been explored. Here, based on overwhelming patterns of genetic, morphological, and ecological data, we reject the hypothesis of a single species broadly distributed throughout Greater Amazonia. Our analyses readily identify three major lineages that diverged during the Miocene and Pliocene— two of which warrant recognition as new species. For one of the new species, we recorded a discharge of 860 V, well above 650 V previously cited for Electrophorus, making it the strongest living bioelectricity generator.

Is there only one electric eel species? Since Linnaeus’s description of Electrophorus electricus 250 years ago, electric eels have fascinated scientists and layperson alike by their capacity to generate strong (~650 V) electric organ discharges (EODs). Strong EODs facilitate hunting, prey capture, and defense, while weaker (~10 V) EODs allow electrolocation and communication. Electric eels inspired the design of Volta’s first electric battery to provide constant current, provide a source of acetylcholinesterase for treating neurodegenerative diseases, and recently encouraged the development of synthetic protocells
with natural nanoconductors and capacitators, and a stacked hydrogel battery that could be used to power medical implants. Electric eels are also an emerging model for genomic studies of animal electrogenesis. Due in part to their large size [up to 2.5m], and specialized electrogenic morphology, electric eels have long been assumed to comprise a single species broadly distributed through Greater Amazonia—the superbasin comprising the Amazon, Orinoco, and coastal drainages of the Guianas e.g., refs.

To test the hypothesis of a single species of Electrophorus, we examine 107 specimens from across Greater Amazonia—including the type locality of E. electricus in Suriname (Supplementary Data 1). To explore species-level divergences, we adopt the General Lineage Concept (GLC), which recognizes species as separately evolving metapopulation lineages. The GLC unifies several pre-existing species concepts, which vary in their criteria for identifying the point of lineage divergence during speciation. Practical applications of the GLC seek multiple, congruent lines of evidence for delimiting species, and to this end we subject a large dataset (comprising mitochondrial and nuclear DNA, morphology, and geographical and ecological distributions) to a range of empirical and model-based procedures. Our analyses lead us to conclude that there are three common species of Electrophorus, which occupy predominantly allopatric ranges (i.e., occupy different regions) in the Guiana Shield (E. electricus), Brazilian Shield (E. voltai sp. nov.) and in the lowland Amazon basin (E. varii sp. nov.). Here we describe these three species, anddiscuss their morphology, evolutionary history, and ecology.

Results and discussion

Genetic analysis. Phylogenetic analyses based on the mitochondrial COI gene resolved three divergent and highly supported lineages corresponding to E. electricus, and the two proposed new species E. voltai, and E. varii—both with Bayesian Inference [posterior probability (PP) >0.95], and Maximum-Likelihood (ML) analysis (bootstrap >0.95; Fig. 1). Estimated evolutionary divergences of COI, using Kimura 2- parameter distances, are: 6.6% between E. electricus and E. voltai; 9.8% between E. electricus and E. varii; and 9.3% between E. voltai and E. varii. Intra-specific ivergences range from 0.02% in E. electricus to 0.31 and 0.32% in E. voltai, and E. varii, respectively. Interspecific COI divergences are also well above the accepted threshold (~2%) used to recognize animal species, including fishes15. Finally, sequences were
analyzed by pairwise distances to assess intra- and interspecific variation, without a priori species hypotheses, using Automatic Barcoding Gap Discovery (ABGD)16. ABGD clustered the sequences into the same three lineages.

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