Electric Fish Research Articles

Evolution of a novel regulatory mechanism of hypoxia inducible factor in hypoxia-tolerant electric fishes

Hypoxia is a significant source of metabolic stress that activates many cellular pathways involved in cellular differentiation, proliferation, and cell death. Hypoxia is also a major component in many human diseases and a known driver of many cancers. Despite the challenges posed by hypoxia, there are animals that display impressive capacity to withstand lethal levels of hypoxia for prolonged periods of time and thus offer a gateway to a more comprehensive understanding of the hypoxic response in vertebrates. The weakly electric fish genus Brachyhypopomus inhabits some of the most challenging aquatic ecosystems in the world, with some species experiencing seasonal anoxia, thus providing a unique system to study the cellular and molecular mechanisms of hypoxia tolerance. In this study, we use closely related species of Brachyhypopomus that display a range of hypoxia tolerances to probe for the underlying molecular mechanisms via hypoxia inducible factors (HIFs)-transcription factors known to coordinate the cellular response to hypoxia in vertebrates. We find that HIF1⍺ from hypoxia tolerant Brachyhypopomus species displays higher transactivation in response to hypoxia than that of intolerant species, when overexpressed in live cells. Moreover, we identified two SUMO-interacting motifs near the oxygen-dependent degradation and transactivation domains of the HIF1⍺ protein that appear to boost transactivation of HIF1, regardless of the genetic background. Together with computational analyses of selection, this shows that evolution of HIF1⍺ are likely to underlie adaptations to hypoxia tolerance in Brachyhypopomus electric fishes, with changes in two SUMO-interacting motifs facilitating the mechanism of this tolerance.

Gene and Allele-Specific Expression Underlying the Electric Signal Divergence in African Weakly Electric Fish.

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.

Ecologically mediated differences in electric organ discharge drive evolution in a sodium channel gene in South American electric fishes.

Active electroreception-the ability to detect objects and communicate with conspecifics via the detection and generation of electric organ discharges (EODs)-has evolved convergently in several fish lineages. South American electric fishes (Gymnotiformes) are a highly species-rich group, possibly in part due to evolution of an electric organ (EO) that can produce diverse EODs. Neofunctionalization of a voltage-gated sodium channel gene accompanied the evolution of electrogenic tissue from muscle and resulted in a novel gene (scn4aa) uniquely expressed in the EO. Here, we investigate the link between variation in scn4aa and differences in EOD waveform. We combine gymnotiform scn4aa sequences encoding the C-terminus of the Nav1.4a protein, with biogeographic data and EOD recordings to test whether physiological transitions among EOD types accompany differential selection pressures on scn4aa. We found positive selection on scn4aa coincided with shifts in EOD types. Species that evolved in the absence of predators, which likely selected for reduced EOD complexity, exhibited increased scn4aa evolutionary rates. We model mutations in the protein that may underlie changes in protein function and discuss our findings in the context of gymnotiform signalling ecology. Together, this work sheds light on the selective forces underpinning major evolutionary transitions in electric signal production.

Open field test for the assessment of anxiety-like behavior in Gnathonemus petersii fish.

The open field test (OFT) is a basic and most widely used test for investigation in animal studies of the neurobiological basis of anxiety and screening for novel drug targets. Here, we present the results of an OFT for weakly electric fish Gnathonemus petersii. This study aimed to describe the behavioral response of G. petersii exposed to an OFT, simultaneously with an evaluation of electrical organ discharges (EOD), to determine whether any association between EOD and patterns of motor behavior in the OFT exists. Treatment of OFT activity and its temporal patterning was assessed for the whole 6-min trial as well as per-minute distributions of activity using a near-infrared camera and an EOD data acquisition system. Our results demonstrated that the time spent, distance moved, and time of activity were significantly higher in the periphery of the OFT arena. The zone preference pattern over the 6-min test session showed that G. petersii prefer the outer zone (83.61%) over the center of the arena (16.39%). The motor behavior of fish measured as distance moved, active time, and swim speed were correlated with the number of EODs; however, no relationship was found between EOD and acceleration.

A Multi-Objective Derived Adaptive TransDeepLabv3 Using Electric Fish Optimization Algorithm for Aerial Image Semantic Segmentation

A Multi-Objective Derived Adaptive TransDeepLabv3 Using Electric Fish Optimization Algorithm for Aerial Image Semantic Segmentation

Androgen receptors rapidly modulate non-breeding aggression in male and female weakly electric fish (Gymnotus omarorum)

The South American weakly electric fish, Gymnotus omarorum, displays territorial aggression year-round in both sexes. To examine the role of rapid androgen modulation in non-breeding aggression, we administered acetate cyproterone (CPA), a potent inhibitor of androgen receptors, to both male and females, just before staged agonistic interactions. Wild-caught fish were injected with CPA and, 30 min later, paired in intrasexual dyads. We then recorded the agonistic behavior which encompasses both locomotor displays and emission of social electric signals. We found that CPA had no discernible impact on the levels of aggression or the motivation to engage in aggressive behavior for either sex. However, CPA specifically decreased the expression of social electric signals in both males and female dyads. The effect was status-dependent as it only affected subordinate electrocommunication behavior, the emission of brief interruptions in their electric signaling (“offs”). This study is the first demonstration of a direct and rapid androgen effect mediated via androgen receptors on non-breeding aggression. Elucidating the mechanisms involved in non-breeding aggression in this teleost model allows us to better understand potentially conserved or convergent neuroendocrine mechanisms underlying aggression in vertebrates.

Diet in phenotypically divergent sympatric species of African weakly electric fish (genus: Campylomormyrus)-A hybrid capture/HTS metabarcoding approach.

Ecological speciation within the mormyrid genus Campylomormyrus resulted in sympatric species exhibiting divergence in their feeding apparatus and electric organ discharge (EOD). This study documents the overall diet of the genus Campylomormyrus and examines the hypothesis that the Campylomormyrus radiation is caused by adaptation to different food sources. We performed diet assessment of five sympatric Campylomormyrus species (C. alces, C. compressirostris, C. curvirostris, C. tshokwe, C. numenius) and their sister taxon Gnathonemus petersii with markedly different snout morphologies and EODs using hybrid capture/HTS DNA metabarcoding of their stomach contents. Our approach allowed for high taxonomic resolution of prey items, including benthic invertebrates, allochthonous invertebrates and vegetation. Comparisons of the diet compositions using quantitative measures and diet overlap indices revealed that all species are able to exploit multiple food niches in their habitats, that is fauna at the bottom, the water surface and the water column. A major part of the diet is larvae of aquatic insects, such as dipterans, coleopterans and trichopterans, known to occur in holes and interstitial spaces of the substrate. The results indicate that different snout morphologies and the associated divergence in the EOD could translate into different prey spectra. This suggests that the diversification in EOD and/or morphology of the feeding apparatus could be under functional adaptation.

A chromosome-level genome of electric catfish (Malapterurus electricus) provided new insights into order Siluriformes evolution.

The online version contains supplementary material available at 10.1007/s42995-023-00197-8.

Long-range and high-precision localization method for underwater bionic positioning system based on joint active–passive electrolocation

Active electrolocation organ of weakly electric fish act as a proximity detection system with high accuracy in recognizing object parameters such as size and shape. In contrast, some fish with passive electrolocation organ are able to detect objects at a greater range. This paper proposes a joint active–passive electrolocation algorithm for long-range and high-precision underwater localization, inspired by the active and passive electroreceptive organs of fish. The study begins by designing a large experimental platform for the underwater localization system to investigate the response of underwater objects to active and passive electric fields. Based on the response, the paper proposes separate underwater active and passive electrolocation algorithms, which are then combined to form a joint algorithm. Experimental results demonstrate that the proposed algorithm achieves high localization accuracy and long detection distance. The joint active–passive electrolocation algorithm has potential applications in submarine resource exploration, underwater robotics, and maritime military projects, while also providing new ideas for future research on long-range underwater object detection and identification based on electrolocation.

The effect of eugenol anesthesia on the electric organ discharge of the weakly electric fish Apteronotus leptorhynchus

Eugenol, the major active ingredient of clove oil, is widely used for anesthesia in fish. Yet virtually nothing is known about its effects on CNS functions, and thus about potential interference with neurophysiological experimentation. To address this issue, we employed a neuro-behavioral assay recently developed for testing of water-soluble anesthetic agents. The unique feature of this in-vivo tool is that it utilizes a readily accessible behavior, the electric organ discharge (EOD), as a proxy of the neural activity generated by a brainstem oscillator, the pacemaker nucleus, in the weakly electric fish Apteronotus leptorhynchus. A deep state of anesthesia, as assessed by the cessation of locomotor activity, was induced within less than 3 min at concentrations of 30–60 µL/L eugenol. This change in locomotor activity was paralleled by a dose-dependent, pronounced decrease in EOD frequency. After removal of the fish from the anesthetic solution, the frequency returned to baseline levels within 30 min. Eugenol also led to a significant increase in the rate of ‘chirps,’ specific amplitude/frequency modulations of the EOD, during the 30 min after the fish’s exposure to the anesthetic. At 60 µL/L, eugenol induced a collapse of the EOD amplitude after about 3.5 min in half of the fish tested. The results of our study indicate strong effects of eugenol on CNS functions. We hypothesize that these effects are mediated by the established pharmacological activity of eugenol to block the generation of action potentials and to reduce the excitability of neurons; as well as to potentiate GABAA-receptor responses.

Vasotocin but not isotocin is involved in the emergence of the dominant-subordinate status in males of the weakly electric fish, Gymnotus omarorum

The establishment of the dominant-subordinate status implies a clear behavioral asymmetry between contenders that arises immediately after the resolution of the agonistic encounter and persists during the maintenance of stable dominance hierarchies. Changes in the activity of the brain social behavior network (SBN) are postulated to be responsible for the establishment and maintenance of the dominant-subordinate status. The hypothalamic nonapeptides of the vasopressin (AVP) and oxytocin (OT) families are known to modulate the activity of the SBN in a context-dependent manner across vertebrates, including status-dependent modulations. We searched for status-dependent asymmetries in AVP-like (vasotocin, AVT) and OT-like (isotocin, IT) cell number and activation immediately after the establishment of dominance in males of the weakly electric fish, Gymnotus omarorum, which displays the best understood example of non-breeding territorial aggression among teleosts. We used immunolabeling (FOS, AVT, and IT) of preoptic area (POA) neurons after dyadic agonistic encounters. This study is among the first to show in teleosts that AVT, but not IT, is involved in the establishment of the dominant-subordinate status. We also found status-dependent subregion-specific changes of AVT cell number and activation. These results confirm the involvement of AVT in the establishment of dominance and support the speculation that AVT is released from dominants' AVT neurons.

Reproductive biology of the electric lanternfish Electrona risso (Myctophidae) and the bigscale fishes Melamphaes polylepis and Scopelogadus mizolepis (Melamphaidae).

This study was the first to investigate the key reproductive traits of the electric lantern fish Electrona risso (Myctophidae, n = 918) and the bigscale fishes (Melamphaidae) Melamphaes polylepis (n = 260) and Scopelogadus mizolepis (n = 649). Specimens of these mesopelagic species were collected in March and April 2015 in the eastern Central Atlantic (0-24° N, 20-26° W). Sex ratio was not significantly different from 1:1 in E. risso and M. polylepis but significantly skewed toward female dominance in S. mizolepis. Reproductive phases were determined macroscopically and by histological analyses on selected individuals. Female length at 50% maturity (L50 ) was 55.1 mm standard length (LS ) in E. risso, with an observed female maximum length (Lmax ) of 81.2 mm LS . M. polylepis females had an L50 of 40.2 mm LS and an Lmax of 86.7 mm LS . S. mizolepis had an L50 of 46 mm LS and an Lmax of 97.9 mm LS . The three species show histological features of iteroparity, but the E. risso population appears to occur in two year-classes and experience only one spawning season per lifetime in the study region. All three species are batch-spawners. A batch fecundity of 2668 eggs was estimated from one E. risso individual, with a relative batch fecundity of 369 eggs g-1 gonad-free body mass. M. polylepis had a batch fecundity of 1027 eggs and a relative batch fecundity of 149 eggs g-1 (n = 3). S. polylepis had a batch fecundity of 1545 eggs and a relative batch fecundity of 215 eggs g-1 (n = 21). The median gonado-somatic index during the actively spawning phase of E. risso was 4.5, significantly lower than that of M. polylepis (7.5) and S. mizolepis (7.1). No regressing or regenerating phases were observed in this study. Batch-spawning in all three species is suggested to be advantageous to cope with intra-annual variability in food supply and other risks for offspring survival. With what appears to be in effect a (facultative) semelparous strategy in combination with a short life span in E. risso, interannual differences would have a great effect on population dynamics of this species. Knowledge is still lacking on temporal aspects of reproduction such as the duration of the spawning season and the frequency of spawning, as well as age and growth.

Gymnotiform electric fishes of the Tres Fronteras region of the western Amazon

Gymnotiform electric knifefishes are an important yet undersampled component of the Neotropical aquatic biota. We report on the gymnotiform fauna of the Tres Fronteras region located at the triple border of Brazil, Colombia, and Peru in the biodiverse western Amazon. The presence of at least 33 species of gymnotiforms in the Tres Fronteras region is validated from recent sampling efforts and the review of previously collected materials. A key is provided for the identification of the species that have been collected from the region. We comment on the diversity of habitat utilization and intraspecific colour variation of some species.

Mode switching in organisms for solving explore-versus-exploit problems

Trade-offs between producing costly movements for gathering information (‘explore’) and using previously acquired information to achieve a goal (‘exploit’) arise in a wide variety of problems, including foraging, reinforcement learning and sensorimotor control. Determining the optimal balance between exploration and exploitation is computationally intractable, necessitating heuristic solutions. Here we show that the electric fish Eigenmannia virescens uses a salience-dependent mode-switching strategy to solve the explore–exploit conflict during a refuge-tracking task in which the same category of movement (fore-aft swimming) is used for both gathering information and achieving task goals. The fish produced distinctive non-Gaussian distributions of movement velocities characterized by sharp peaks for slower, task-oriented ‘exploit’ movements and broad shoulders for faster ‘explore’ movements. The measures of non-normality increased with increased sensory salience, corresponding to a decrease in the prevalence of fast explore movements. We found the same sensory salience-dependent mode-switching behaviour across ten phylogenetically diverse organisms, from amoebae to humans, performing tasks such as postural balance and target tracking. We propose a state-uncertainty-based mode-switching heuristic that reproduces the distinctive velocity distribution, rationalizes modulation by sensory salience and outperforms the classic persistent excitation approach while using less energy. This mode-switching heuristic provides insights into purposeful exploratory behaviours in organisms, as well as a framework for more efficient state estimation and control of robots.

Brain and circulating steroids in an electric fish: Relevance for non-breeding aggression.

Steroids play a crucial role in modulating brain and behavior. While traditionally it is thought that the brain is a target of sex steroids produced in endocrine glands (e.g. gonads), the brain itself produces steroids, known as neurosteroids. Neurosteroids can be produced in regions involved in the regulation of social behaviors and may act locally to regulate social behaviors, such as reproduction and aggression. Our model species, the weakly electric fish Gymnotus omarorum, displays non-breeding aggression in both sexes. This is a valuable natural behavior to understand neuroendocrine mechanisms that differ from those underlying breeding aggression. In the non-breeding season, circulating sex steroid levels are low, which facilitates the study of neurosteroids. Here, for the first time in a teleost fish, we used liquid chromatography-tandem mass spectrometry (LC-MS/MS) to quantify a panel of 8 steroids in both plasma and brain to characterize steroid profiles in wild non-breeding adult males and females. We show that: 1) systemic steroid levels in the non-breeding season are similar in both sexes, although only males have detectable circulating 11-ketotestosterone, 2) brain steroid levels are sexually dimorphic, as females display higher levels of androstenedione, testosterone and estrone, and only males had detectable 11-ketotestosterone, 3) systemic androgens such as androstenedione and testosterone in the non-breeding season are potential precursors for neuroestrogen synthesis, and 4) estrogens, which play a key role in non-breeding aggression, are detectable in the brain (but not the plasma) in both sexes. These data are consistent with previous studies of G. omarorum that show non-breeding aggression is dependent on estrogen signaling, as has also been shown in bird and mammal models. Overall, our results provide a foundation for understanding the role of neurosteroids, the interplay between central and peripheral steroids and potential sex differences in the regulation of social behaviors.

Unraveling the complex phylogeographic history of freshwater fishes in Lower Central America: A study of the electric fish Brachyhypopomus occidentalis

Lower Central America (LCA) has a complex biogeographic history shaped by the rise of the Isthmus of Panama and the global climatic oscillations of the Pleistocene. These events have been crucial in structuring biodiversity in LCA, but their consequences for the distribution and partitions of genetic diversity across the region remain to be elucidated. We combined complete mitochondrial genomes and nuclear ultraconserved elements (UCEs) to study the phylogeographic history and population genetic structure of the electric fish Brachyhypopomus occidentalis in LCA. Our results are consistent with the known phylogeographic history of B. occidentalis in LCA, but we update this history in several important ways that help illuminate the phylogeographic history of freshwater fishes in the region. We provide: i) support for three waves of colonization, two of which occurred prior to the final closure of the Panama Isthmus; ii) a more precise understanding of each colonization event, with evidence for a larger footprint of the first event, as well as genetic exchange across the continental divide in subsequent events; and iii) evidence for high levels of previously unrecognized population genetic structure across LCA. This updated model of colonization and diversification of B. occidentalis consists of three waves of dispersal and colonization, which triggered the evolution of geographic breaks in both nuclear and mitochondrial genomes across LCA. These processes are tightly linked to the dynamic uplift of the Isthmus, recent volcanic activity in the region, and the sea-level oscillations of the Pleistocene. These results improve previous phylogeographic inferences regarding the distribution and diversification of freshwater fishes in LCA, and generate testable hypotheses to guide future research exploring the factors shaping biodiversity in the region.

Virtual chemical analysis and machine learning-based prediction of polyethylene terephthalate nanoplastics toxicity on aquatic organisms as influenced by particle size and properties

This study focuses on the chemical analysis and prediction of Polyethylene Terephthalate (PET) toxicity, considering the influence of particle size and properties. The effect PET of different sizes (1, 4, 9, 16 and 25 nm coded NP1 to NP5) on aquatic organisms such as Terpedo californica (electric ray fish) and Danio rerio (zebrafish) as model species was evaluated by virtual chemical techniques and machine learning methodology based on Multilayer Perceptrons Artificial Neural Networks (MLP ANN) and Support Vector Machine. The PET NPs was built and characterized in silico and then docked on the acetylcholinesterase (TcAChE) and cytochrome P450 (Zf CYP450) of the organisms, respectively. The results showed that the binding affinities of the NPs increased steadily from – 7.1 kcal mol-1 to – 9.9 kcal mol-1 for NP1 to NP4 and experienced a drop at NP5 (– 8.9 kcal mol-1) for TcAChE. The Zf CYP450 also had a similar pattern ranging from -5.2 kcal mol-1 to -8.1 kcal mol-1. The MLP ANN showed an accuracy of 85.9 % and 77.3 %. In comparison, SVM showed a better PET NPs toxicity prediction with an accuracy of 99.5 % and 99.4% based on the inherent properties of TcAChE and Zf CYP450, respectively.

EAEFA: An Efficient Energy-Aware Task Scheduling in Cloud Environment

The scheduling of tasks in the cloud is a major challenge for improving resource availability and decreasing the total execution time and energy consumption of operations. Due to its simplicity, efficiency, and effectiveness in identifying global optimums, electric fish optimisation (EFO) has recently garnered a lot of interest as a metaheuristic method for solving optimisation issues. In this study, we apply electric fish optimisation (EAEFA) to the problem of cloud task scheduling in an effort to cut down on power usage and turnaround time. The objective is to finish all tasks in the shortest possible time, or makespan, taking into account constraints like resource availability and task dependencies. In the EAEFA approach, a school of electric fish is used to solve a multi-objective optimization problem that represents the scheduling of tasks. Because electric fish are drawn to high-quality solutions and repelled by low-quality ones, the algorithm is able to converge to a global optimum. Experiments validate EAEFA's ability to solve the task scheduling issue in cloud computing. The suggested scheduling strategy was tested on HPC2N and other large-scale simulations of real-world workloads to measure its makespan time, energy efficiency and other performance metrics. Experimental results demonstrate that the proposed EAEFA method improves performance by more than 30% with respect to makespan time and more than 20% with respect to overall energy consumption compared to state-of-the-art methods.

BECS-II: an updated bio-inspired electrocommunication system for small underwater robots.

Some weakly electric fish can use electric signals to interact and communicate with each other in dark and complex underwater environments where traditional underwater communication fails. In our previous work, we developed a bio-inspired electrocommunication system (BECS) that serves as an effective alternative to traditional methods in this challenging underwater scenario performing communication at a speed of approximately 1200 bps (bits per second) within approximately 3 m. In this study, a novel underwater wireless communication system (BECS-II) is proposed to upgrade the BECS with much better performance. We first propose theoretical and simulation models for electrocommunication, including the effects of the angular frequency and electrode impedance. A custom-made digital communication system is employed in BECS-II to improve the anti-interference ability and channel capacity of the BECS. In addition, a novel circuit optimization strategy was used to develop a customized circuit to enhance the transmitting and receiving capabilities of the BECS-II. Dual-frequency communication is proposed to meet the communication demands of different tasks by taking inspiration from the task allocation and evolution mechanisms of weakly electric fish. The experimental results showed that BECS-II outperformed BECS in high-frequency mode at both the communication speed (approximately 20 kbps) and distance (approximately 10 m), whereas in low-frequency mode, it extended the communication range by transmitting data up to a distance of approximately 20 m at a speed of approximately 200 bps. A substantial increase in the communication distance can expand the robot motion space in a group and improve group flexibility.&#xD.

Weakly electric fish use self-generated motion to discriminate object shape

Weakly electric fish use self-generated motion to discriminate object shape