Communication can contribute to the evolution of biodiversity by promoting speciation and reinforcing reproductive isolation between existing species. The evolution of species-specific signals depends on the ability of individuals to detect signal variation, which in turn relies on the capability of the brain to process signal information. Here, we show that evolutionary change in a region of the brain devoted to the analysis of communication signals in mormyrid electric fishes improved detection of subtle signal variation and resulted in enhanced rates of signal evolution and species diversification. These results show that neural innovations can drive the diversification of signals and promote speciation.

Several species of Mormyrid weakly electric fish have a mobile chin protuberance that serves as a mobile antenna during prey detection, tracking behaviors, and foraging for food. It has been proposed that it constitutes a fovea of the electrosensory system. The distribution of the three types of receptor organs involved in active imaging of the local surroundings, prey detection, and passive electroreception, and their central projection to the electrosensory lobe (ELL), have been studied in Gnathonemus petersii. Density distributions were compared for different body regions. Primary afferent projections were labeled with biocytin or biotinylated dextrans. This showed that there is considerable central "over-representation" of the mandibular and nasal regions of the sensory surface involved in electrolocation, at the expense of the other body regions investigated. This over-representation is not a mere effect of the very high density of receptor organs in these areas, but is found to be due to central magnification. This magnification differs between the subclasses of electroreceptors, suggesting a functional segregation in the brain. We conclude that the chin protuberance and the nasal region are the regions of greatest sensitivity for the resistive, capacitive, and low-frequency characteristics of the environment, and are probably most important in prey detection, whereas other regions of the skin with a lesser resolution and sensitivity to phase distortion of the EOD, in particular the trunk, are probably designed for imaging larger, inanimate features of the environment. Our data support the hypothesis that the chin appendage and nasal region are functionally distinct electrosensory foveae.

SUMMARYWeakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation, nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance, can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response (novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions -the Schnauzenorgan and the nasal region -can be termed electric fovea but they serve separate functions during active electrolocation.

No abstract

SUMMARY Peripheral filtering is a fundamental mechanism for establishing frequency tuning in sensory systems. By contrast, detection of temporal features, such as duration, is generally thought to result from temporal coding in the periphery, followed by an analysis of peripheral response times within the central nervous system. We investigated how peripheral filtering properties affect the coding of stimulus duration in the electrosensory system of mormyrid fishes using behavioral and electrophysiological measures of duration tuning. We recorded from individual knollenorgans, the electrosensory receptors that mediate communication, and found correlated variation in frequency tuning and duration tuning, as predicted by a simple circuit model. In response to relatively high intensity stimuli, knollenorgans responded reliably with fixed latency spikes, consistent with a temporal code for stimulus duration. At near-threshold intensities, however, both the reliability and the temporal precision of responses decreased. Evoked potential recordings from the midbrain, as well as behavioral responses to electrosensory stimulation, revealed changes in sensitivity across the range of durations associated with the greatest variability in receptor sensitivity. Further, this range overlapped with the natural range of variation in species-specific communication signals, suggesting that peripheral duration tuning affects the coding of behaviorally relevant stimuli. We measured knollenorgan, midbrain and behavioral responses to natural communication signals and found that each of them were duration dependent. We conclude that at relatively low intensities for which temporal coding is ineffective, diversity among sensory receptors establishes a population code, in which duration is reflected in the population of responding knollenorgans.