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African mormyrid fishes are by far the most diverse group of osteoglossomorph (bony tongue) fishes. Mormyrids communicate using pulses of electricity, and they process electric communication signals in the midbrain exterolateral nucleus (EL). In its ancestral form, the EL is relatively small and homogenous. In two different lineages, however, the EL expanded in size and increased in cytological complexity. This evolutionary change established the perceptual ability to distinguish variation in electric pulse waveform, which plays an important role in species recognition and mate choice. However, the sensory basis of social behavior in species with a small, homogenous EL remains unknown. Using published species descriptions, we found that species in one of these lineages have relatively large eyes. Using sectioned brains, we measured the volume of a major visual region, the optic tectum (OT), and found that this same lineage also has an enlarged OT. We also found that eye size and OT size are highly correlated across species. Phylogenetic analysis suggests that a reduced visual system evolved with the origins of an active electrosense, and that this one particular lineage secondarily evolved an enlarged visual system. Behavioral tests revealed that this enlargement of the visual system established increased visual acuity. Thus, our findings demonstrate that different lineages of mormyrids have evolved visual or electrosensory specializations, but that no lineages have specialized in both. This sensory divergence likely reflects fundamentally different ecologies and suggests that vision may play an especially important role in the social behavior of mormyrids that cannot detect variation in electric signal waveform. Our findings provide an example of evolutionary change in multiple sensory systems among closely related species that lays a foundation for relating ecological adaptation to evolutionary change in multisensory perception and social behavior.

Independent Evolution of Visual and Electrosensory Specializations in Different Lineages of Mormyrid Electric Fishes