02068nas a2200157 4500008004100000245015900041210006900200260001600269520141200285100001701697700002101714700002501735700002201760700002301782856010501805 2020 eng d00aGenetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fish Paramormyrops kingsleyae0 aGenetic drift does not sufficiently explain patterns of electric cJan-04-20213 a

Communication signals serve crucial survival and reproductive functions. In Gabon, the widely distributed mormyrid fish Paramormyrops kingsleyae emits an electric organ discharge (EOD) signal with a dual role in communication and electrolocation that exhibits remarkable variation: populations of P. kingsleyae have either biphasic or triphasic EODs, a feature that characterizes interspecific signal diversity among the Paramormyrops genus. We quantified variation in EODs of 327 P. kingsleyae from nine populations and compared it to genetic variation estimated from microsatellite loci. We found no correlation between electric signal and genetic distances, suggesting that EOD divergence cannot be explained by drift alone. An alternative hypothesis is that EOD differences are used for mate discrimination, which would require P. kingsleyae be capable of differentiating between divergent EOD waveforms. Using a habituation-dishabituation assay, we found that P. kingsleyae can discriminate between biphasic and triphasic EOD types. Nonetheless, patterns of genetic and electric organ morphology divergence provide evidence for hybridization between these signal types. Although reproductive isolation with respect to signal type is incomplete, our results suggest that EOD variation in P. kingsleyae could be a cue for assortative mating.

1 aPicq, Sophie1 aSperling, Joshua1 aCheng, Catherine, J.1 aCarlson, Bruce, A1 aGallant, Jason, R. uhttp://doi.wiley.com/10.1111/evo.13953https://onlinelibrary.wiley.com/doi/am-pdf/10.1111%2Fevo.1395303260nas a2200157 4500008004100000022001400041245012600055210006900181260001600250300001100266520262900277100002202906700001902928700002202947856013302969 2019 eng d a0006-897700aSensory Specializations of Mormyrid Fish Are Associated with Species Differences in Electric Signal Localization Behavior0 aSensory Specializations of Mormyrid Fish Are Associated with Spe cJan-03-2019 a1 - 173 a

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.

1 aVélez, Alejandro1 aRyoo, Da, Yeon1 aCarlson, Bruce, A uhttps://www.karger.com/Article/FullText/496493https://www.karger.com/Article/Pdf/496493https://www.karger.com/Article/Pdf/49649303433nas a2200181 4500008004100000022001400041245011700055210006900172260002000241300001600261490000700277520282600284100001803110700001103128700002203139700002203161856006803183 2016 eng d a0270-647400aBehavioral and Single-Neuron Sensitivity to Millisecond Variations in Temporally Patterned Communication Signals0 aBehavioral and SingleNeuron Sensitivity to Millisecond Variation cFeb-16-20162220 a8985 - 90000 v363 a

In many sensory pathways, central neurons serve as temporal filters for timing patterns in communication signals. However, how a population of neurons with diverse temporal filtering properties codes for natural variation in communication signals is unknown. Here we addressed this question in the weakly electric fish Brienomyrus brachyistius, which varies the time intervals between successive electric organ discharges to communicate. These fish produce an individually stereotyped signal called a scallop, which consists of a distinctive temporal pattern of ∼8–12 electric pulses. We manipulated the temporal structure of natural scallops during behavioral playback and in vivo electrophysiology experiments to probe the temporal sensitivity of scallop encoding and recognition. We found that presenting time-reversed, randomized, or jittered scallops increased behavioral response thresholds, demonstrating that fish's electric signaling behavior was sensitive to the precise temporal structure of scallops. Next, using in vivo intracellular recordings and discriminant function analysis, we found that the responses of interval-selective midbrain neurons were also sensitive to the precise temporal structure of scallops. Subthreshold changes in membrane potential recorded from single neurons discriminated natural scallops from time-reversed, randomized, and jittered sequences. Pooling the responses of multiple neurons improved the discriminability of natural sequences from temporally manipulated sequences. Finally, we found that single-neuron responses were sensitive to interindividual variation in scallop sequences, raising the question of whether fish may analyze scallop structure to gain information about the sender. Collectively, these results demonstrate that a population of interval-selective neurons can encode behaviorally relevant temporal patterns with millisecond precision.

SIGNIFICANCE STATEMENT The timing patterns of action potentials, or spikes, play important roles in representing information in the nervous system. However, how these temporal patterns are recognized by downstream neurons is not well understood. Here we use the electrosensory system of mormyrid weakly electric fish to investigate how a population of neurons with diverse temporal filtering properties encodes behaviorally relevant input timing patterns, and how this relates to behavioral sensitivity. We show that fish are behaviorally sensitive to millisecond variations in natural, temporally patterned communication signals, and that the responses of individual midbrain neurons are also sensitive to variation in these patterns. In fact, the output of single neurons contains enough information to discriminate stereotyped communication signals produced by different individuals.

1 aBaker, C., A.1 aMa, L.1 aCasareale, C., R.1 aCarlson, Bruce, A uhttp://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.0648-16.201601591nas a2200133 4500008004100000245012000041210006900161260001600230490000600246520110100252100002201353700002201375856006001397 2016 eng d00aDetection of transient synchrony across oscillating receptors by the central electrosensory system of mormyrid fish0 aDetection of transient synchrony across oscillating receptors by cSep-06-20170 v53 a

Recently, we reported evidence for a novel mechanism of peripheral sensory coding based on oscillatory synchrony. Spontaneously oscillating electroreceptors in weakly electric fish (Mormyridae) respond to electrosensory stimuli with a phase reset that results in transient synchrony across the receptor population (Baker et al., 2015). Here, we asked whether the central electrosensory system actually detects the occurrence of synchronous oscillations among receptors. We found that electrosensory stimulation elicited evoked potentials in the midbrain exterolateral nucleus at a short latency following receptor synchronization. Frequency tuning in the midbrain resembled peripheral frequency tuning, which matches the intrinsic oscillation frequencies of the receptors. These frequencies are lower than those in individual conspecific signals, and instead match those found in collective signals produced by groups of conspecifics. Our results provide further support for a novel mechanism for sensory coding based on the detection of oscillatory synchrony among peripheral receptors.

1 aVélez, Alejandro1 aCarlson, Bruce, A uhttp://elifesciences.org/lookup/doi/10.7554/eLife.1685102363nas a2200145 4500008004100000022001400041245013300055210006900188260001600257300001200273490000800285520184500293100002202138856005702160 2016 eng d a0022-094900aDifferences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes0 aDifferences in electrosensory anatomy and social behavior in an  cApr-11-2016 a31 - 430 v2193 a

Sensory systems play a key role in social behavior by mediating the detection and analysis of communication signals. In mormyrid fishes, electric signals are processed within a dedicated sensory pathway, providing a unique opportunity to relate sensory biology to social behavior. Evolutionary changes within this pathway led to new perceptual abilities that have been linked to increased rates of signal evolution and species diversification in a lineage called ‘clade A’. Previous field observations suggest that clade-A species tend to be solitary and territorial, whereas non-clade-A species tend to be clustered in high densities suggestive of schooling or shoaling. To explore behavioral differences between species in these lineages in greater detail, I studied population densities, social interactions, and electric signaling in two mormyrid species, Gnathonemus victoriae (clade A) and Petrocephalus degeni (non-clade A), from Lwamunda Swamp, Uganda. Petrocephalus degeni was found at higher population densities, but intraspecific diversity in electric signal waveform was greater in G. victoriae. In the laboratory, G. victoriae exhibited strong shelter-seeking behavior and competition for shelter, whereas P. degeni were more likely to abandon shelter in the presence of conspecifics as well as electric mimics of signaling conspecifics. In other words, P. degeni exhibited social affiliation whereas G. victoriae exhibited social competition. Further, P. degeni showed correlated electric signaling behavior whereas G. victoriae showed anti-correlated signaling behavior. These findings extend previous reports of social spacing, territoriality, and habitat preference among mormyrid species, suggesting that evolutionary divergence in electrosensory processing relates to differences in social behavior.

1 aCarlson, Bruce, A uhttp://jeb.biologists.org/cgi/doi/10.1242/jeb.12772002572nas a2200169 4500008004100000022001400041245012100055210006900176260001600245300001400261490000700275520199800282100002602280700002602306700002202332856004802354 2013 eng d a0006-897700aIndependent Evolution of Visual and Electrosensory Specializations in Different Lineages of Mormyrid Electric Fishes0 aIndependent Evolution of Visual and Electrosensory Specializatio cJan-01-2013 a185 - 1980 v823 a

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.

1 aStevens, Jennifer, A.1 aSukhum, Kimberley, V.1 aCarlson, Bruce, A uhttp://www.karger.com?doi=10.1159/00035536900430nas a2200121 4500008004100000245007800041210006900119300001400188490000800202100002500210700002200235856005100257 2005 eng d00aElectric organ discharge patterns during group hunting by a mormyrid fish0 aElectric organ discharge patterns during group hunting by a morm a1305-13140 v2721 aArnegard, Matthew, E1 aCarlson, Bruce, A uhttps://mormyrids.efishgenomics.com/fr/node/4301506nas a2200133 4500008004100000245008200041210006900123300001400192490000600206520105200212100002201264700002501286856006101311 2011 eng d00aNeural innovations and the diversification of African weakly electric fishes.0 aNeural innovations and the diversification of African weakly ele a720–7250 v43 a

In African mormyrid fishes, evolutionary change in a sensory region of the brain established an ability to detect subtle variation in electric communication signals. In one lineage, this newfound perceptual ability triggered a dramatic increase in the rates of signal evolution and species diversification. This particular neural innovation is just one in a series of nested evolutionary novelties that characterize the sensory and motor systems of mormyrids, the most speciose group of extant osteoglossomorph fishes. Here we discuss the behavioral significance of these neural innovations, relate them to differences in extant species diversity, and outline possible scenarios by which some of these traits may have fueled diversification. We propose that sensory and motor capabilities limit the extent to which signals evolve and, by extension, the role of communication behavior in the process of speciation. By expanding these capabilities, neural innovations increase the potential for signal evolution and species diversification.

1 aCarlson, Bruce, A1 aArnegard, Matthew, E uhttp://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?