Sensory Specializations of Mormyrid Fish Are Associated with Species Differences in Electric Signal Localization Behavior

Abstract

The ability to localize communication signals plays a fundamental role in social interactions. For signal localization to take place, the sensory system of the receiver must extract information about distance and direction to the sender from physical characteristics of the signal. In many sensory systems, information from multiple peripheral receptors must be integrated by central sensory pathways to determine the sender location. Here, we asked whether evolutionary divergence in the electrosensory and visual systems of mormyrid fish is associated with signal localization behavior. In mormyrids, differences in the distribution of electroreceptors on the surface of the skin are associated with differences in the midbrain exterolateral nucleus (EL). Species with electroreceptors clustered in three rosettes on both sides of the head have a small and undifferentiated EL. In contrast, EL is enlarged and subdivided into anterior (ELa) and posterior (ELp) regions in species that have electroreceptors broadly ­distributed throughout the body. Interestingly, species with EL and clustered electroreceptors also have larger visual systems and higher visual acuity than species with ELa/ELp and broadly distributed electroreceptors. Species with broadly distributed electroreceptors and ELa/ELp approached a simulated conspecific by following the curved electric field lines generated by the electrosensory stimulus. In contrast, a species with small EL and clustered electroreceptors, but an enlarged visual system, followed shorter and straighter paths to the stimulus source. In the central electrosensory system, evoked field potentials in response to stimuli delivered from the left versus the right differed more in EL than in ELa/ELp. Our results suggest that signal localization behavior is associated with differences in sensory specializations. We propose that the distribution of electroreceptors on the body affects the ability of individuals to align parallel to electric field lines and maintain such alignment while approaching the signal source. The spatial resolution of sensory information relayed from the periphery to the midbrain in species with clustered electroreceptors may allow for gross, but not fine, processing of sender location. Furthermore, visual information may play an important role in localizing signaling individuals in species with small EL and clustered electroreceptors. In line with previous studies, we suggest that the physiological and behavioral differences associated with signal localization reflect adaptations to different habitats and social environments.