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Markham, M. R.

Publications and source records attributed to Markham, M. R..

4 recordsLinked to original sources

Electrosensory and metabolic responses of weakly electric fish to changing water conductivity

Weakly electric Gymnotiform fishes use self-generated electric organ discharges (EODs) to navigate and communicate. The electrosensory range for these processes is a function of EOD amplitude, determined by the fishs electric organ (EO) output and the electrical conductivity of the surrounding water. Anthropogenic activity, such as deforestation, dams, and industrial/agricultural runoff, are known to increase water conductivity in neotropical habitats, likely reducing the electrosensory range of these fish. We investigated whether fish modulate EO output as means of re-expanding electrosensory range after a rapid increase in water conductivity in the pulse-type Brachyhypopomus gauderio and the wave-type Eigenmannia virescens. Furthermore, because EOD production incurs significant metabolic costs, we assessed whether such compensation is associated with an increase in metabolic rate. Following the conductivity increase B. gauderio increased EOD amplitude by 20.2 {+/-} 4.3% over six days but with no associated increase in metabolic rate, whereas the EOD amplitude of E. virescens remained constant, accompanied by an unexpected decrease in metabolic rate. Our results suggest that B. gauderio uses a compensation mechanism that requires no metabolic investment, such as impedance matching, or a physiological tradeoff wherein energy is diverted from other physiological processes to increase EO output. These divergent responses between species could be the result of differences in reproductive life history or evolutionary adaptations to different aquatic habitats. Continued investigation of electrosensory responses to changing water conditions will be essential for understanding the effects of anthropogenic disturbances on gymnotiforms, and potential physiological mechanisms for adapting to a rapidly changing aquatic environment.

physiology↗

Spike-frequency dependent coregulation of multiple ionic conductances in fast-spiking cells forces a metabolic tradeoff

High-frequency action potentials (APs) allow rapid information acquisition and processing in neural systems, but create biophysical and metabolic challenges for excitable cells. The electric fish Eigenmannia virescens images its world and communicates with high-frequency (200-600 Hz) electric organ discharges (EODs) produced by synchronized APs generated at the same frequency in the electric organ cells (electrocytes). We cloned three previously unidentified Na+-activated K+ channel isoforms from electroctyes (eSlack1, eSlack2, and eSlick1). In electrocytes, mRNA transcript levels of the rapidly-activating eSlick, but not the slower eSlack1 or eSlack2, correlated with EOD frequency across individuals. In addition, transcript levels of an inward-rectifier K+ channel, a voltage-gated Na+ channel, and Na+,K+-ATPases also correlated with EOD frequency while a second Na+ channel isoform did not. Computational simulations showed that maintaining electrocyte AP waveform integrity as firing rates increase requires scaling conductances in accordance with these mRNA expression correlations, causing AP metabolic costs to increase exponentially.

neuroscience↗

Derived loss of signal complexity and plasticity in a genus of weakly electric fish

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. We discuss potential the roles of signal mimicry, species recognition, and sexual selection in maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.

physiology↗

Electrostatic Tuning of a Potassium Channel in Electric Fish

Molecular and biophysical variation contributes to the evolution of adaptive phenotypes, particularly behavior, though it is often difficult to understand precisely how. The adaptively significant electric organ discharge behavior of weakly electric fish is the direct result of biophysical membrane properties set by ion channels. Here we describe a voltage-gated potassium channel gene in African mormyrid electric fishes, that is under positive selection and highly expressed in the electric organ. The channel produced by this gene shortens electric organ action potentials by activating quickly and at hyperpolarized membrane potentials. Surprisingly, the source of these unique properties is a derived patch of negatively charged amino acids in an extracellular loop near the voltage sensor. Further, we demonstrate that this portion of the channel functions differently in vertebrates than the generally accepted model based on the shaker channel, and suggest a role for this loop in the evolutionary tuning of voltage-dependent channels.

evolutionary biology↗