Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes

Brain region size generally scales allometrically with total brain size, but mosaic shifts in brain region size independent of brain size have been found in several lineages and may be related to the evolution of behavioral novelty. African weakly electric fishes (Mormyroidea) evolved a mosaically enlarged cerebellum and hindbrain, yet the relationship to their behaviorally novel electrosensory system remains unclear. We addressed this by studying South American weakly electric fishes (Gymnotiformes) and weakly electric catfishes (Synodontis spp.), which evolved varying aspects of electrosensory systems, independent of mormyroids. If the mormyroid mosaic increases are related to evolving an electrosensory system, we should find similar mosaic shifts in gymnotiforms and Synodontis. Using micro-computed tomography scans, we quantified brain region scaling for multiple electrogenic, electroreceptive, and non-electrosensing species. We found mosaic increases in cerebellum in all three electrogenic lineages relative to non-electric lineages and mosaic increases in torus semicircularis and hindbrain associated with the evolution of electrogenesis and electroreceptor type. These results show that evolving novel electrosensory systems is repeatedly and independently associated with changes in the sizes of individual brain regions independent of brain size, which suggests that selection can impact structural brain composition to favor specific regions involved in novel behaviors.

Electric eels galore: microsatellite markers for population studies

Fourteen novel microsatellite loci are described and characterized in two species of electric eels, Electrophorus variiand E. voltaifrom floodplains and rivers of the Amazon rainforest. These loci are polymorphic, highly informative, and have the capacity to detect reliable levels of genetic diversity. Likewise, the high combined probability of paternity exclusion value and low combined probability of genetic identity value obtained demonstrate that the new set of loci displays suitability for paternity studies on electric eels. In addition, the cross-amplification of electric eel species implies that it may also be useful in the study of the closely related E. electricus, and to other Neotropical electric fishes (Gymnotiformes) species as tested herein.

Convergent patterns of evolution of mitochondrial oxidative phosphorylation (OXPHOS) genes in electric fishes

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’.

Spooky interaction at a distance in cave and surface dwelling electric fishes

ABSTRACTGlass knifefish (Eigenmannia) are a group of weakly electric fishes found throughout the Amazon basin. We made recordings of the electric fields of two populations of freely behaving Eigenmannia in their natural habitats: a troglobitic population of blind cavefish (Eigenmannia vicentespelaea) and a nearby epigean (surface) population (Eigenmannia trilineata). These recordings were made using a grid of electrodes to determine the movements of individual fish in relation to their electrosensory behaviors. The strengths of electric discharges in cavefish were larger than in surface fish, which may be a correlate of increased reliance on electrosensory perception and larger size. Both movement and social signals were found to affect the electrosensory signaling of individual Eigenmannia. Surface fish were recorded while feeding at night and did not show evidence of territoriality. In contrast, cavefish appeared to maintain territories. Surprisingly, we routinely found both surface and cavefish with sustained differences in electric field frequencies that were below 10 Hz despite being within close proximity of less than one meter. A half century of analysis of electrosocial interactions in laboratory tanks suggest that these small differences in electric field frequencies should have triggered the jamming avoidance response. Fish also showed significant interactions between their electric field frequencies and relative movements at large distances, over 1.5 meters, and at high differences in frequencies, often greater than 50 Hz. These interactions are likely envelope responses in which fish alter their EOD frequency in relation to changes in the depth of modulation of electrosocial signals.