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Convergent Designs for Electrogenesis and Electroreception Convergent designs for electrogenesis and electroreception Carl D Hopkins Cornell University, Ithaca, USA New- and old-world tropical electric fish lack a common electrical ancestor, suggesting that the mechanisms of signal generation and recognition evolved independently in the two groups. Recent research on convergent designs for electrogenesis and electroreception has focused on the structure of electric organs, the neural circuitry controlling the pacemaker driving the electric organ, and the neural circuitry underlying time coding of electric waveforms. Current Opinion in Neurobiology 1995, 5:769-777 Introduction (Osteoglossomorpha, Teleostei) from Africa and the Gymnotiformes (Ostariophysi, Teleostei) from South Ethologists and neuroethologists have been fascinated America, are distantly related but do not share a common by electric fish and by the evolution of an entirely electrogenic or electroreceptive ancestor 12,121; however, novel electrosensory modality ever since Hans Lissmann’s each of these two groups has a sister group of fish discovery of ‘weak electrogenesis’ in the monnyriform that has arnpullary electroreceptors but no electric fishes of Africa in 1951 [l] and his subsequent discovery organs [4,12]. In spite of the phylogenetic distance, of active electrolocation (the sensing of objects in the both the mormyrifornls and gynmotifornls include environment as distortions in the electric field generated wave- and pulse-discharging species. I3oth groups have by a fish’s own electric organ discharge) [2,3]. We pulse-discharging species that generate complex electric now know that the electric sense is used for electrical organ discharge (EOD) waveforms. They also both have communication [4-6,7”], for passive electrical sensing three types of electroreceptors with distinct functions of prey [8], and for active electrolocation [9,10]. and separate pathways, and both use their electric organs for electrolocation and communication. Electric fish provide a good model system in neuro- ethology for several reasons: there are many species The parallels between the two groups run even deeper to compare in new- and old--world groups; electric when looking at the cellular basis for behavior. Several behavior is novel and inherently fascinating; the modality new studies [15-191 have explored the mechanisms is convenient to work with physiologically; and there of electrogcnesis, particularly the production of con- are many parallels between the electric sense and plcx EOD waveforms. As an electric discharge is audition Ill]. This review focuses on recent research an electrostatic field and not a propagating wave, that examines convergent designs for electrogenesis and EOD waveforms are unaffected by echo, reverberation, electroreception in new- and old-world fresh-water refraction, reflection or any other phenomenon affecting tropic.11 fish. propagating waves (such as sound) [ 131. Gymnotiform electric organs Phylolgeny and electrogenesis Dut how does the electric organ generate something more complex than a simple, biphasic, spike-like Key to any comparative neurobiological study is a good discharge that one would expect from the sequential comprehension of the phylogenetic relationship between activation of the caudal and the rostra1 faces of the organisnu in question, and the recent explosive simple electrocytes [14]! Some of the South American growth of cladistics coillbined with new molecular gynmotiforms, such as Gyrtmtrrs rrlmpo, can generate techniques has had a clear ilnpact on the field of a triphasic EOD by firing a subset of electrocytes neuroethology. It is now clear that the two main slightly out of phase with the rest of the population group:; of fresh-water electric fish, the Mornlyriformes [l&19]. Electrocytes near the head have a specialized Abbreviations AMPA-cc-amino-3-hydroxy--5-methyl-4-isoxazole proprionic acid; BCA nucleus-bulbar command-associated nucleus; ELa--exterolateralis pars anterior: ELL-Glectrosensory lateral line lobe; ELvxterolateralis pars posterior; EOD-electric organ discharge; CABA--y-aminobutyric acid; ICL-inner cellular layer; ITD-interaural time difference; MRN-medullary relay nucleus: NMDA-N-methyl-D-aspartate; PPn-pre-pacemaker nucleus; PPn-c-‘chirp’ part of the diencephalic PPn; PPn-g--gradual frequency shift region of the PPn; SPPn-sub-lemniscal PPn. 0 Current Biology Ltd ISSN 0959-4388 769 770 Neural control the fish in these four genera produce complex EOD (b) EOD waveforms containing three or even four major peaks waveform (Fig. lb). By contrast, fish in the genera Bra~hyllypoporrrfrs (formerly Hypopotwus) and Microstcrnarchus do not appear to have accessory electric organs, and their EODs are (iii) very simple, being composed of biphasic waveforms. The revised phylogeny based on molecular data shows that these complex accessory electric organs may have had a single common evolutionary origin rather than multiple unrelated origins, as suggested by the traditional (0 phylogeny. ~ (ii) 04 EODs , ~ -1/ Brachyhypopomus j _ Fig. 1. Complex EOD waveforms generated by a South American electric fish. (a) The gymnotiform Gymnotus carapo generates (b) a complex EOD waveform with four components: (i) an early gradual head negativity, (ii) a strong head-negative peak, (iii) a head-positive peak, and (iv) a head-negative peak. The head-positive peak (iii) re- sults from the synchronous discharge of the posterior faces of the majority of the electrocytes in tubes 2, 3 and 4 of cells in the elec- tric organ, which receive innervation from the anterior or poste- rior electromotor nerves. The final head negativity (iv) arises from the inward current through the anterior faces of these same elec- trocytes, which have become depolarized by the passive current flow through them from the posterior face. Early head negativity (i) is caused by inward current through the anterior faces of the elec- trocytes in tube 1; these are innervated on the anterior side from nerves with a shorter conduction time to the electric organ. These specialized electrocytes generate a local head-negative discharge, which precedes the’main EOD in the tail. Adapted from 1151. anterior innervation in addition to the typical posterior one, plus a shorter conduction pathway from the pacemaker. This ensures that the rostra1 faces of the electrocytes fire first, making the head negative; this occurs before the electric organ in the tail, which Fig. 2. A recent phylogenetic analysis of the gymnotiform elec .. is caudally innervated, goes head-positive and then tric fish of South America derived from analysis of sequences of mitochondrial DNA. This analysis demonstraies a closk relation- negative again (Fig. 1) [15]. An elegant series of recent ship between the genera Rhamphichthys, Gymnorhamphichthys, papers details the complexity of the electric organs in Steatogenys, and Hy~_‘opygus, whereas previous traditional mor- Gyrrrnot~s carapo and the patterns of innervation and phological studies had placed the last two closer to Brachyhy- motor control [15-191. Other gymnotiforms, such as popomus and Microsternarchus in a separate family (Hypopomi- dae; !ight shading). The revised phylogenetic analysis is consistent Stcatqcnys elegans, Hypopygus lepk4rus and Rhanrphichthys with the common presence of accessory electric organs in Hypopy- achieve multi-phased EODs using electrocytes located in gus, Steatogenys, Cymnorhamphichthys and Rhamphichthys. The accessory electric organs on the underside of the head accessory electric organs found on the underside of the head are re- sponsible for generating the early head-negative phase of the EOD [14], in addition to the main organ in the tail. (indicated by arrows). Adapted from [20**]. Heterogeneous electric organs, accessory electric organs and simple electric organs are more interesting when viewed in the light of phylogeny. Alves-Games et al. [20*] used mitochondrial DNA to construct a Mormyrid electric organs phylogeny for the gymnotiform electric fish of South The 200 species of African mormyrids are well America to re-examine relationships among the pulse known for their EOD diversity [5,21] and for gener- gymnotiforms (Fig. 2). Pulse discharges appear to ating monophasic, biphasic, triphasic, inverted tripha- have arisen independently in the families Gymnotidae sic and even four-phase EOD waveforms (Fig. 3). (Gymwotus) and Electrophoridae (Electrophoms), and Recently, Alves-Games and Hopkins (J Alves-Games, then again in the Hypopomidae/Rhamphichthyidae CD Hopkins, unpublished data) generated a partial families. Especially interesting is the apparent clade phylogeny of the A&can mormyriform electric fishes composed of the genera Gyttrnorhatrrphichfhys, Rhatrr- using mitochondrial DNA, and the phylogeny was phichthys, Hypopyg14s and Stcatqerrys, all of which have used as a framework to re-examine the evolution of accessory electric organs in addition to the more their complex electrocyte morphology (Fig. 4). The typical electric organ located in the long tail. All molecular phylogeny suggests that primitive electric Convergent designs for electrogenesis and electroreception Hopkins 771 (a) Stalkless (b) Non-penetrating (c) Penetrating stalk, (d) Inverted (e) Doubly penetrating stalk, posterior anterior penetrating and non-penetrating innervation innervation stalk, posterior stalk innervation EODs -- &______;,_______+;;o&_____:_ Petrocephalus Brienomyrus Morm yrops Pollimyrus bovei sp. 5 zanclirostris isidori Fig. 3. The electric organs of the mormyriforms are composed of electrocytes
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