Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes

Abstract

Polymorphism in an animal communication channel provides a framework for studying proximate rules of signal design as well as ultimate mechanisms of signal diversification. Reproductively isolated mormyrid fishes from Gabon's Brienomyrus species flock emit distinctive electric organ discharges (EODs) thought to function in species and sex recognition. Species boundaries and EODs appear congruent in these fishes, with the notable exception of three morphs designated types I, II and III. Within the species flock, these morphs compose a monophyletic group that has recently been called the magnostipes complex. Co-occurring morphs of this complex express distinctive EODs, yet they appear genetically indistinguishable at several nuclear loci. In this study, we investigated EOD discrimination by these morphs using both behavioral and physiological experiments. During the breeding season, wild-caught type I and type II males showed evidence that they can discriminate their own morph's EOD waveform from that of a sympatric and genetically distinct reference species. However, we found that type I and type II males exhibited an asymmetry in unconditioned responses to paired playback of EODs recorded from type I versus type II females. Males of the type II morph responded preferentially to EODs of type II females, whereas type I males did not appear to discriminate homotypic and heterotypic EODs in our experimental paradigm. Part of this behavioral asymmetry may have resulted from a previously undetected difference in adult size, which may have enhanced apparent discrimination by the smaller morph (type II) due to a relatively higher risk of injury from the larger morph (type I). Knollenorgan receptors, which mediate electrical communication in mormyrids, showed similar spectral tuning in type I and type II. These electroreceptors coded temporal features of any single magnostipes-complex EOD with similar patterns of time-locked spikes in both morphs. By contrast, Knollenorgans exhibited distinctive responses to different EOD waveforms. These results suggest that discrete EOD variation in this rapidly diversifying complex is functional in terms of morph-specific advertisement and recognition. Time-domain signal divergence has outpaced frequency-domain divergence between sympatric morphs, requiring little to no change in receptor response properties. We discuss our findings in light of a model for EOD time-coding by the Knollenorgan pathway, as well as evolutionary hypotheses concerning sympatric signal diversification in the magnostipes complex.