Molecular evolution of the ependymin-related gene epdl2 in African weakly electric fish.

Gene duplication and subsequent molecular evolution can give rise to taxon-specific gene specializations. In previous work, we found evidence that African weakly electric fish (Mormyridae) may have as many as three copies of the epdl2 gene, and the expression of two epdl2 genes is correlated with electric signal divergence. Epdl2 belongs to the ependymin-related family (EPDR), a functionally diverse family of secretory glycoproteins. In this study, we first describe vertebrate EPDR evolution and then present a detailed evolutionary history of epdl2 in Mormyridae with emphasis on the speciose genus Paramormyrops. Using Sanger sequencing, we confirm three apparently functional epdl2 genes in Paramormyrops kingsleyae. Next, we developed a nanopore-based amplicon sequencing strategy and bioinformatics pipeline to obtain and classify full-length epdl2 gene sequences (N = 34) across Mormyridae. Our phylogenetic analysis proposes three or four epdl2 paralogs dating from early Paramormyrops evolution. Finally, we conducted selection tests which detected positive selection around the duplication events and identified ten sites likely targeted by selection in the resulting paralogs. These sites' locations in our modeled 3D protein structure involve four sites in ligand binding and six sites in homodimer formation. Together, these findings strongly imply an evolutionary mechanism whereby epdl2 genes underwent selection-driven functional specialization after tandem duplications in the rapidly speciating Paramormyrops. Considering previous evidence, we propose that epdl2 may contribute to electric signal diversification in mormyrids, an important aspect of species recognition during mating.

A dynamic spike threshold with correlated noise predicts observed patterns of negative interval correlations in neuronal spike trains.

Negative correlations in the sequential evolution of interspike intervals (ISIs) are a signature of memory in neuronal spike-trains. They provide coding benefits including firing-rate stabilization, improved detectability of weak sensory signals, and enhanced transmission of information by improving signal-to-noise ratio. Primary electrosensory afferent spike-trains in weakly electric fish fall into two categories based on the pattern of ISI correlations: non-bursting units have negative correlations which remain negative but decay to zero with increasing lags (Type I ISI correlations), and bursting units have oscillatory (alternating sign) correlation which damp to zero with increasing lags (Type II ISI correlations). Here, we predict and match observed ISI correlations in these afferents using a stochastic dynamic threshold model. We determine the ISI correlation function as a function of an arbitrary discrete noise correlation function [Formula: see text], where k is a multiple of the mean ISI. The function permits forward and inverse calculations of the correlation function. Both types of correlation functions can be generated by adding colored noise to the spike threshold with Type I correlations generated with slow noise and Type II correlations generated with fast noise. A first-order autoregressive (AR) process with a single parameter is sufficient to predict and accurately match both types of afferent ISI correlation functions, with the type being determined by the sign of the AR parameter. The predicted and experimentally observed correlations are in geometric progression. The theory predicts that the limiting sum of ISI correlations is [Formula: see text] yielding a perfect DC-block in the power spectrum of the spike train. Observed ISI correlations from afferents have a limiting sum that is slightly larger at [Formula: see text] ([Formula: see text]). We conclude that the underlying process for generating ISIs may be a simple combination of low-order AR and moving average processes and discuss the results from the perspective of optimal coding.

Electric-field-coupled oscillators for collective electrochemical perception in biohybrid robotics.

This work explores the application of nonlinear oscillators coupled by an electric field in water, inspired by weakly electric fish. Such coupled oscillators operate in clear and colloidal (mud, bottom silt) water and represent a collective electrochemical sensor that is sensitive to global environmental parameters, the geometry of the common electric field and spatial dynamics of autonomous underwater vehicles (AUVs). Implemented in hardware and software, this approach can be used to create global awareness in a group of robots, which possess limited sensing and communication capabilities. Using oscillators from different AUVs enables extension of the range limitations related to the electric dipole of a single AUV. Applications of this technique are demonstrated for detecting the number of AUVs, distances between them, perception of dielectric objects and synchronization of behavior. Recognizing self-/nonself-generated signals by electric fish is re-embodied in a technological way through an 'electrical mirror' for discrimination between 'collective self' and 'collective nonself'. These approaches have been implemented in several research projects with bioinspired/biohybrid systems in fresh and salt water, and electrochemical sensing in fluidic media.

Development of an underwater networking system using bio-inspired electrocommunication.

Current underwater communication typically includes acoustic, optical, radio frequency, and magneto-inductive channels. Wireless sensor networks are usually built on these four channels. However, these underwater networks are vulnerable to complex aquatic environments. In nature, weakly electric fish are able to communicate electrically (called electrocommunication), which is 'invisible' to most other animals, to convey information such as species, courtship, and environmental conditions. Inspired by the electrocommunication of weakly electric fish, an artificial electrocommunication system that uses an electric induction (EI) channel has been developed recently. This paper further develops an underwater networking system using the EI channel, which addresses the solutions to collision avoidance and routing problems during electrocommunication networking. In particular, a CSMA/CA-based electrocommunication mechanism was used to solve the collision problem. Then, a single-hop underwater electrocommunication network (UEN) was established. Furthermore, a complex multi-hop UEN was implemented on the basis of the ad hoc on-demand distance vector routing protocol. Theoretical analysis, simulations, and experiments were conducted to demonstrate the effectiveness of the developed UEN. Extensive results show that the UEN holds the potential to serve as a complement to future underwater wireless sensor networks.

Minimal sensor arrays for localizing objects using an electric sense.

Weakly electric fish encode perturbations in a self-generated electric field to sense their environment. Localizing objects using this electric sense requires that distance be decoded from a two-dimensionalelectric imageof the field perturbations on their skin. Many studies of object localization by weakly electric fish, and by electric sensing in a generic context, have focused on extracting location information from different features of the electric image. Some of these studies have also considered the additional information gained from sampling the electric image at different times, and from different viewpoints. Here, we take a different perspective and instead consider the information available at asinglepoint in space (i.e. a single sensor or receptor) at a single point in time (i.e. constant field). By combining the information from multiple receptors, we show that an object's distance can be unambiguously encoded by as few as four receptors at specific locations on a sensing surface in a manner that is relatively robust to environmental noise. This provides a lower bound on the information (i.e. receptor array size) required to decode the three-dimensional location of an object using an electric sense.

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

Brain region size generally scales allometrically with 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 major brain regions independent of brain size, suggesting that selection can impact structural brain composition to favor specific regions involved in novel behaviors.

Larger animals tend to have larger brains and smaller animals tend to have smaller ones. However, some species do not fit the pattern that would be expected based on their body size. This variation between species can also apply to individual brain regions. This may be due to evolutionary forces shaping the brain when favouring particular behaviours. However, it is difficult to directly link changes in species behaviour and variations in brain structure. One way to understand the impact of evolutionary adaptations is to study species that have developed new behaviours and compare them to related ones that lack such a behaviour. An opportunity to do this lies in the ability of several species of fish to produce and sense electric fields in water. While this system is not found in most fish, it has evolved multiple times independently in distantly-related lineages. Schumacher and Carlson examined whether differences in the size of brains and individual regions between species were associated with the evolution of electric field generation and sensing. Micro-computed tomography, or µCT, scans of the brains of multiple fish species revealed that the species that can produce electricity ­ also known as 'electrogenic' species' ­ have more similar brain structures to each other than to their close relatives that lack this ability. The brain regions involved in producing and detecting electrical charges were larger in these electrogenic fish. This similarity was apparent despite variations in how total brain size has evolved with body size across species. These results demonstrate how evolutionary forces acting on particular behaviours can lead to predictable changes in brain structure. Understanding how and why brains evolve will allow researchers to better predict how species' brains and behaviours may adapt as human activities alter their environments.

Underwater robot coordination using a bio-inspired electrocommunication system.

Due to the challenging communication and control systems, few underwater multi-robot coordination systems are currently developed. In nature, weakly electric fish can organize their collective activities using electrocommunication in turbid water. Inspired by this communication mechanism, we developed an artificial electrocommunication system for underwater robots in our previous work. In this study, we coordinate a group of underwater robots using this bio-inspired electrocommunication. We first design a time division multiple access (TDMA) network protocol for electrocommunication to avoid communication conflicts during multi-robot coordination. Then, we revise a distributed controller to coordinate a group of underwater robots. The distributed controller on each robot generates the required controls based on adjacent states obtained through electrocommunication. A central pattern generator (CPG) controller is designed to adjust the speed of individuals according to distributed control law. Simulations and experimental results show that a group of underwater robots is able to achieve coordination with the developed electrocommunication and control systems.

Electrocommunication signals and aggressive behavior vary among male morphs in an apteronotid fish, Compsaraia samueli.

Within-species variation in male morphology is common among vertebrates and is often characterized by dramatic differences in behavior and hormonal profiles. Males with divergent morphs also often use communication signals in a status-dependent way. Weakly electric knifefish are an excellent system for studying variation in male morphology and communication and its hormonal control. Knifefish transiently modulate the frequency of their electric organ discharge (EOD) during social encounters to produce chirps and rises. In the knifefish Compsaraia samueli, males vary extensively in jaw length. EODs and their modulations (chirps and rises) have never been investigated in this species, so it is unclear whether jaw length is related to the function of these signals. We used three behavioral assays to analyze EOD modulations in male C. samueli: (1) artificial playbacks, (2) relatively brief, live agonistic dyadic encounters, and (3) long-term overnight recordings. We also measured circulating levels of two androgens, 11-ketotestosterone and testosterone. Chirp structure varied within and across individuals in response to artificial playback, but was unrelated to jaw length. Males with longer jaws were more often dominant in dyadic interactions. Chirps and rises were correlated with and preceded attacks regardless of status, suggesting these signals function in aggression. In longer-term interactions, chirp rate declined after 1 week of pairing, but was unrelated to male morphology. Levels of circulating androgens were low and not predictive of jaw length or EOD signal parameters. These results suggest that communication signals and variation in male morphology are linked to outcomes of non-breeding agonistic contests.

Neural readout of a latency code in the active electrosensory system.

The latency of spikes relative to a stimulus conveys sensory information across modalities. However, in most cases, it remains unclear whether and how such latency codes are utilized by postsynaptic neurons. In the active electrosensory system of mormyrid fish, a latency code for stimulus amplitude in electroreceptor afferent nerve fibers (EAs) is hypothesized to be read out by a central reference provided by motor corollary discharge (CD). Here, we demonstrate that CD enhances sensory responses in postsynaptic granular cells of the electrosensory lobe but is not required for reading out EA input. Instead, diverse latency and spike count tuning across the EA population give rise to graded information about stimulus amplitude that can be read out by standard integration of converging excitatory synaptic inputs. Inhibitory control over the temporal window of integration renders two granular cell subclasses differentially sensitive to information derived from relative spike latency versus spike count.

Is the Medium the Message? Functional Diversity Across Abiotic Gradients in Freshwater Electric Fishes.

Evolutionary transitions across abiotic gradients can occur among habitats at multiple spatial scales, and among taxa and biotas through a range of ecological and evolutionary time frames. Two diverse groups of electric fishes, Neotropical Gymnotiformes, and Afrotropical Mormyroidea, offer interesting examples of potentially convergent evolution in aspects of morphological, physiological, and life history traits. We examined biogeographical, morphological, and functional patterns across these two groups to assess the degree of convergence in association with abiotic environmental variables. While there are superficial similarities across the groups and continents, we found substantially more differences in terms of habitat occupancy, electric signal diversity, and morphological disparity. These differences likely correlate to differences in biogeographical histories across the Neotropics and Afrotropics, biotic factors associated with aquatic life and electric signals, and sampling issues plaguing both groups. Additional research and sampling are required to make further inferences about how electric fishes transition throughout diverse freshwater habitats across both microevolutionary and macroevolutionary scales.

Morphology and receptive field organization of a temporal processing region in Apteronotus albifrons.

The timing system of weakly electric fishes is vital for many behavioral processes, but the system has been relatively unexplored in Apteronotus albifrons. This paper describes the receptive fields of phase-locked neurons in the midbrain of A. albifrons, in combination with neuroanatomy and electron microscopy (EM) to delineate a phase-locked area in this fish, the magnocellular mesencephalic nucleus (MMN). The MMN was isolated electrophysiologically through the detection of phase-locked field potentials of high amplitude. Single-cell recordings were made with a sharp electrode while a phase-locked modulated stimulus was provided to the fish. Receptive field centers of phase-locked neurons in MMN were consistent with tuberous electroreceptor density maps from previous studies, but no receptive field centers were found in the posterior 50% of the body. Intracellular and extracellular labeling of MMN revealed three cell populations: giant cells with large somata (19-24 µm) and their axonal arborizations which span across the entire extent of MMN, axon terminals from spherical cells of the electrosensory lateral line lobe (ELL), and small cell somata (3-7 µm) along with their projections which extend outside the nucleus. EM revealed multiple gap junction and chemical synapses within MMN. Our results indicate that MMN is a dedicated temporal processing center in A. albifrons.

Intergenus F1-hybrids of African weakly electric fish (Mormyridae: Gnathonemus petersii ♂ × Campylomormyrus compressirostris ♀) are fertile.

Hybridisation is an important element of adaptive radiation in fish but data are limited in weakly electric mormyrid fish in this respect. Recently, it has been shown that intragenus hybrids (Campylomormyrus) are fertile and are able to produce F2-fish. In this paper, we demonstrate that even intergenus hybrids (Gnathonemus petersii ♂ × Campylomormyrus compressirostris ♀) are fertile. Three artificial reproduction (AR) trials, with an average fertilisation rate of ca. 23%, yielded different numbers of survivals (maximally about 50%) of the F1-hybrids. The complete ontogenetic development of these hybrids is described concerning their morphology and electric organ discharge (EOD). Two EOD types emerged at the juvenile stage, which did not change up to adulthood. Type I consisted of four phases and Type II was triphasic. The minimum body length at sexual maturity was between 10 and 11 cm. Malformations, growth and mortality rates are also described.

Phylogenomics of Bony-Tongue Fishes (Osteoglossomorpha) Shed Light on the Craniofacial Evolution and Biogeography of the Weakly Electric Clade (Mormyridae).

Bonytongues (Osteoglossomorpha) constitute an ancient clade of teleost fishes distributed in freshwater habitats throughout the world. The group includes well-known species such as arowanas, featherbacks, pirarucus, and the weakly electric fishes in the family Mormyridae. Their disjunct distribution, extreme morphologies, and electrolocating capabilities (Gymnarchidae and Mormyridae) have attracted much scientific interest, but a comprehensive phylogenetic framework for comparative analysis is missing, especially for the species-rich family Mormyridae. Of particular interest are disparate craniofacial morphologies among mormyrids which might constitute an exceptional model system to study convergent evolution. We present a phylogenomic analysis based on 546 exons of 179 species (out of 260), 28 out of 29 genera, and all six families of extant bonytongues. Based on a recent reassessment of the fossil record of osteoglossomorphs, we inferred dates of divergence among transcontinental clades and the major groups. The estimated ages of divergence among extant taxa (e.g., Osteoglossomorpha, Osteoglossiformes, and Mormyroidea) are older than previous reports, but most of the divergence dates obtained for clades on separate continents are too young to be explained by simple vicariance hypotheses. Biogeographic analysis of mormyrids indicates that their high species diversity in the Congo Basin is a consequence of range reductions of previously widespread ancestors and that the highest diversity of craniofacial morphologies among mormyrids originated in this basin. Special emphasis on a taxon-rich representation for mormyrids revealed pervasive misalignment between our phylogenomic results and mormyrid taxonomy due to repeated instances of convergence for extreme craniofacial morphologies. Estimation of ancestral phenotypes revealed contingent evolution of snout elongation and unique projections from the lower jaw to form the distinctive Schnauzenorgan. Synthesis of comparative analyses suggests that the remarkable craniofacial morphologies of mormyrids evolved convergently due to niche partitioning, likely enabled by interactions between their exclusive morphological and electrosensory adaptations. [Africa; ancestral state estimation; diversity; exon capture; freshwater fishes; Phylogenomics.].

Neural processing: Cracking the code to extract relevant social information.

How does the brain decode sensory features from social signals? A new study in electric fish provides an elegant model where mixed selectivity coding and corollary discharges at the thalamic level can guide decision making in social behavior.

Mixed selectivity coding of sensory and motor social signals in the thalamus of a weakly electric fish.

High-level neural activity often exhibits mixed selectivity to multivariate signals. How such representations arise and modulate natural behavior is poorly understood. We addressed this question in weakly electric fish, whose social behavior is relatively low dimensional and can be easily reproduced in the laboratory. We report that the preglomerular complex, a thalamic region exclusively connecting midbrain with pallium, implements a mixed selectivity strategy to encode interactions related to courtship and rivalry. We discuss how this code enables the pallial recurrent networks to control social behavior, including dominance in male-male competition and female mate selection. Notably, response latency analysis and computational modeling suggest that corollary discharge from premotor regions is implicated in flagging outgoing communications and thereby disambiguating self- versus non-self-generated signals. These findings provide new insights into the neural substrates of social behavior, multi-dimensional neural representation, and its role in perception and decision making.

Salience of multisensory feedback regulates behavioral variability.

Many animal behaviors are robust to dramatic variations in morphophysiological features, both across and within individuals. The control strategies that animals use to achieve such robust behavioral performances are not known. Recent evidence suggests that animals rely on sensory feedback rather than precise tuning of neural controllers for robust control. Here we examine the structure of sensory feedback, including multisensory feedback, for robust control of animal behavior. We re-examined two recent datasets of refuge tracking responses ofEigenmannia virescens, a species of weakly electric fish.Eigenmanniarely on both the visual and electrosensory cues to track the position of a moving refuge. The datasets include experiments that varied the strength of visual and electrosensory signals. Our analyses show that increasing the salience (perceptibility) of visual or electrosensory signals resulted in more robust and precise behavioral responses. Further, we find that robust performance was enhanced by multisensory integration of simultaneous visual and electrosensory cues. These findings suggest that engineers may achieve better system performance by improving the salience of multisensory feedback rather than solely focusing on precisely tuned controllers.

Communication with self, friends and foes in active-sensing animals.

Animals that rely on electrolocation and echolocation for navigation and prey detection benefit from sensory systems that can operate in the dark, allowing them to exploit sensory niches with few competitors. Active sensing has been characterized as a highly specialized form of communication, whereby an echolocating or electrolocating animal serves as both the sender and receiver of sensory information. This characterization inspires a framework to explore the functions of sensory channels that communicate information with the self and with others. Overlapping communication functions create challenges for signal privacy and fidelity by leaving active-sensing animals vulnerable to eavesdropping, jamming and masking. Here, we present an overview of active-sensing systems used by weakly electric fish, bats and odontocetes, and consider their susceptibility to heterospecific and conspecific jamming signals and eavesdropping. Susceptibility to interference from signals produced by both conspecifics and prey animals reduces the fidelity of electrolocation and echolocation for prey capture and foraging. Likewise, active-sensing signals may be eavesdropped, increasing the risk of alerting prey to the threat of predation or the risk of predation to the sender, or drawing competition to productive foraging sites. The evolutionary success of electrolocating and echolocating animals suggests that they effectively counter the costs of active sensing through rich and diverse adaptive behaviors that allow them to mitigate the effects of competition for signal space and the exploitation of their signals.

Motion parallax for object localization in electric fields.

Parallax, as a visual effect, is used for depth perception of objects. But is there also the effect of parallax in the context of electric field imagery? In this work, the example of weakly electric fish is used to investigate how the self-generated electric field that these fish utilize for orientation and communication alike, may be used as a template to define electric parallax. The skin of the electric fish possesses a vast amount of electroreceptors that detect the self-emitted dipole-like electric field. In this work, the weakly electric fish is abstracted as an electric dipole with a sensor line in between the two emitters. With an analytical description of the object distortion for a uniform electric field, the distortion in a dipole-like field is simplified and simulated. On the basis of this simulation, the parallax effect could be demonstrated in electric field images i.e. by closer inspection of voltage profiles on the sensor line. Therefore, electric parallax can be defined as the relative movement of a signal feature of the voltage profile (here, the maximum or peak of the voltage profile) that travels along the sensor line peak trace (PT). The PT width correlates with the object's vertical distance to the sensor line, as close objects create a large PT and distant objects a small PT, comparable with the effect of visual motion parallax.

Immunohistochemical description of isotocin neurons and the anatomo-functional comparative analysis between isotocin and vasotocin systems in the weakly electric fish, Gymnotus omaroum.

The vasopressin-vasotocin (AVP-AVT) and oxytocin-mesotocin-isotocin (OT-MT-IT) families of nonapeptides are of great importance in shaping context-dependent modulations of a conserved and yet highly plastic network of brain areas involved in social behavior: the social behavior network. The nonapeptide systems of teleost fish are highly conserved and share a common general organization. In this study, we first describe the presence of IT cells and projections in the brain of an electric fish, Gymnotus omarorum. Second, we confirm that IT neuron types and distribution in the preoptic area (POA) follow the same general pattern previously described in other teleost species. Third, we show that although IT and AVT neurons occur intermingled within the POA of G. omarorum and can be classified into the same subgroups, they present subtle but remarkable differences in size, number, and location. Finally, we show that unlike AVT, IT has no effect on basal electric signaling, reinforcing the specificity in the actions that each one of these nonapeptides has on social behavior and communication.