Abstract

The communication behaviors of vocal fish and electric fish are among the vertebrate social behaviors best understood at the level of neural circuits. Both forms of signaling rely on midbrain inputs to hindbrain pattern generators that activate peripheral effectors (sonic muscles and electrocytes) to produce pulsatile signals that are modulated by frequency/repetition rate, amplitude and call duration. To generate signals that vary by sex, male phenotype, and social context, these circuits are responsive to a wide range of hormones and neuromodulators acting on different timescales at multiple loci. Bass and Zakon (2005) reviewed the behavioral neuroendocrinology of these two teleost groups, comparing how the regulation of their communication systems have both converged and diverged during their parallel evolution. Here, we revisit this comparison and review the complementary developments over the past 16 years. We (a) summarize recent work that expands our knowledge of the neural circuits underlying these two communication systems, (b) review parallel studies on the action of neuromodulators (e.g., serotonin, AVT, melatonin), brain steroidogenesis (via aromatase), and social stimuli on the output of these circuits, (c) highlight recent transcriptomic studies that illustrate how contemporary molecular methods have elucidated the genetic regulation of social behavior in these fish, and (d) describe recent studies of mochokid catfish, which use both vocal and electric communication, and that use both vocal and electric communication and consider how these two systems are spliced together in the same species. Finally, we offer avenues for future research to further probe how similarities and differences between these two communication systems emerge over ontogeny and evolution.

Highlights

  • The neuroendocrine mechanisms underlying social behavior are daunting in their complexity

  • The frequency and timing of these sounds or electric organ discharges (EODs) vary by sex and male phenotype, and such variations are regulated largely by hormones acting as modulators in a coordinated but independent manner at multiple loci in the motor circuit

  • We focus on several key neural and endocrine processes that have been researched recently in both teleost systems and make direct comparisons to highlight how these analogous communication systems have evolved similar and different mechanisms

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Summary

INTRODUCTION

The neuroendocrine mechanisms underlying social behavior are daunting in their complexity. In 2005, two of us (Bass and Zakon, 2005) reviewed the behavioral neuroendocrinology of distantly related teleost groups (see Nelson et al, 2016) that produce either vocalizations or electric organ discharges (EODs) and compared how their communication systems have both converged and diverged during their parallel evolution. The frequency and timing of these sounds or EODs vary by sex and male phenotype (e.g., type I and II male morphs of sonic midshipman fish), and such variations are regulated largely by hormones acting as modulators in a coordinated but independent manner at multiple loci in the motor circuit We revisit this comparison and review what has been learned in the intervening 16 years. We describe recent studies of mochokid catfish that produce both vocal and electric signals and consider how these two systems can be spliced together and regulated in the same species

BRIEF OVERVIEW OF VOCAL AND ELECTRIC SIGNALING IN FISH
Vocal Fish
Electric Fish
NEURAL CIRCUITS UNDERLYING VOCAL AND ELECTRIC SIGNALING
Neural Circuitry Generating Vocal and Electric Signals
Neural Circuitry for Reception of Vocal and Electric Signals
NEUROMODULATORY AND HORMONAL REGULATION OF COMMUNICATION AND SOCIAL BEHAVIOR
Arginine Vasotocin
Regulation of Diel Patterns of Signaling
Social Regulation of Steroids and Communication Behavior
CONTRIBUTIONS OF MOLECULAR STUDIES TO THE NEUROETHOLOGY OF SOCIAL BEHAVIOR
Organization of Motor System in Catfish
Evolutionary Patterns in Vocal and Electric Communication in Catfish
FUTURE DIRECTIONS
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