Topic: Electric fish: insights into convergence
Ever seen an electric eel in an aquarium? Don’t dare putting your hand in the tank...
A number of animals have independently evolved electroreception – they are capable of perceiving weak electric currents with the help of specialised receptors. This passive electric sense is found in many fish, several amphibians and monotreme mammals and useful for obstacle avoidance or prey detection. Some fish, however, have gone one step further and evolved an active electric sense. They can not only receive electric signals, but also generate electric fields themselves with the help of an electric organ. Not surprisingly, this electrogenesis, which is employed for electrocommunication, active electrolocation or, in the case of strong electric discharges, even for stunning prey or predators, is convergent as well…
Groups of electric fish
Electrogenesis has evolved independently in at least six lineages of teleosts and elasmobranchs, which can be subdivided into strongly and weakly electric fish according to the power of their electric discharge.
Strongly electric fish
Several dozen species of fish are capable of generating strong electric fields, with the electric eel (Electrophorus electricus) probably being the best-known example. This South American freshwater dweller, which stuns prey with electric shocks of up to 500 volts, is, in fact, not a true eel, but a Neotropical knifefish (Gymnotiformes). Powerful electrogenesis is also known from the marine electric rays (Torpediniformes), particularly the torpedoes (genus Torpedo), after which the naval weapon has been named, the tropical electric catfish (Malapteruridae) and the stargazers (Uranoscopidae). These perciform fish bury themselves in sand and have a modified skull so that their eyes, nostrils and most of the mouth are above the sand when submerged. Stargazers such as Astroscopus have an electric organ located behind the eyes that is derived from modified extra-ocular muscles, and they discharge electric currents of up to 50 volts in defence.
Weakly electric fish
There are several hundred species of fish that produce electric discharges in the range between millivolts and a few volts. All marine skates in the family Rajidae and some African catfish in the genera Synodontis and Clarias are weakly electric, but far better studied are two speciose lineages that present remarkable examples of convergence. The Mormyriformes (which comprise the Mormyridae or elephantfish and the Gymnarchidae with Gymnarchus niloticus as the only species) flourish in the rivers and lakes of Africa, while the Gymnotiformes (or Neotropical knifefish) inhabit South American freshwaters. Phylogenetic analysis clearly shows that they are only distantly related and that their strikingly similar mechanisms of signal generation and recognition have thus evolved completely separately.
Electric organs (EOs) are usually located on the tail or along the side of the body, and some species possess accessory EOs on the head. In most electric fish, they consist of bunches of modified, non-contractile muscle fibres arranged in a stack. Members of the family Apteronidae, however, have an EO that is neural in origin. The specialised muscle or nerve cells in the EO (electrocytes) are innervated on one side, which creates a potential difference (similar to a battery). The potentials are summed and delivered simultaneously to the surrounding water as an electric organ discharge (EOD). Not surprisingly, the EOs of strongly electric fish are huge and contain a large number of electrocytes.
There are several types of EOs that differ in electrocyte morphology. For mormyrids, it has been suggested that electrocytes with penetrating stalks have evolved once from non-penetrating stalked electrocytes and that there have been several independent reversals to this ancestral condition.
EODs can either be pulse- or wave-type patterns. Pulse-type EODs are brief, often multi-phasic pulses emitted at irregular intervals, and the discharge rate increases when the fish is active. Wave-type fish produce longer-duration, often monophasic pulses that form a sine wave-like pattern. Independent of their activity, they discharge constantly within a certain frequency band. EODs show great diversity (e.g. in duration or frequency) between and often also within species. This diversity is related to their various functions and based on physiological differences, for example in the type, density and distribution of ion channels in electrocyte membranes or in the mode of EO innervation.
While all strongly electric fish produce pulse-type EODs, those of weakly electric fish can either be of the pulse or wave type. Wave discharges and pulse discharges with complex waveforms have evolved in both the mormyriforms and gymnotiforms and within the latter, pulse-type EODs have probably arisen independently in several families. Particularly striking parallels are found between the gymnotiform Eigenmannia and the mormyriform Gymnarchus, which both produce wave discharges between 300 and 500 Hz, short EOD interruptions during aggressive acts and slight frequency modulations as displays of submission. Interestingly, gymnotiforms and mormyriforms that are preyed upon by electroreceptive catfish or electric eels have adjusted the frequency of their EODs to minimise the risk of detection by these predators.
Neural control mechanisms
The electromotor control system of mormyriforms and gymnotiforms is quite well understood. In both groups, discharge patterns are generated by a hierarchy of control nuclei in the medulla, the midbrain and the thalamus. The electromotor control areas in their brains show many parallels, but because this is a convergence, the detailed pathways differ. For example, in both groups a nucleus in the ventral medulla that consists of electrically coupled and thus synchronously firing cells triggers firing of the EO. However, this structure is referred to as a pacemaker nucleus in the gymnotiforms (as it spontaneously generates a regular rhythm), while in mormyriforms it is termed a command nucleus (as it integrates external synaptic inputs and does not show a pacemaker-like regularity). Both these nuclei project via a medullary relay nucleus to the electromotor nucleus in the spinal cord, the neurons of which innervate the electrocytes in the EO.
It is important to emphasise that inputs from other sensory modalities, such as lateral line, visual and auditory pathways, are integrated and thus affect the generation of EODs in gymnotiforms and mormyrids. This integration of signals has parallels in other groups, such as the dolphins, which combine sensory inputs from both vision and echolocation, or infrared-sensitive snakes, which overlay thermal and visual images. Such integrations have interesting implications for cognitive processes.
EOD pulses depend on ion (particularly Na+) currents, which are generated by ion channels. Whilst mammals possess ten Na+ channel genes, seven to eight were found in teleosts. It is considered likely that the common ancestor of teleosts and tetrapods had four, which were then duplicated at the origin of teleosts. Fish possess two duplicate copies of the mammalian muscle Na+ channel gene Nav1.4, Nav1.4a and Nav1.4b, which are both expressed in the muscles of non-electric fish. In electric fish, however, Nav1.4a expression has been lost in muscle and independently been gained in the EOs of mormyriforms and gymnotiforms (with the exception of adult apteronotids, which have a neurally-derived EOs). This change in role might have freed Nav1.4a from selective constraints acting on its evolution in muscle (where mutations are usually detrimental) and allowed for elevated rates of amino acid substitutions in electric fish. These substitutions have occurred convergently in domains that affect the inactivation of the channel, a factor that is vital in shaping EODs and likely to be related to EOD diversity. Thus, the evolution of EOs and diversity in EODs in mormyriforms and gymnotiforms was accompanied by convergent molecular changes.
All electric fish with the exception of stargazers can not only generate but also perceive electric fields with sensitive electroreceptors. These receptors are usually widely distributed over the body surface but more densely clustered around the head. Three different types of electroreceptor have been detected in fish – all comprise a sensory epithelium composed of transducer cells that convert external electrical stimuli into internal neural responses, but then differ in their structure and function.
Ampullary receptors, where the sensory epithelium is at the base of a jelly-filled canal that opens to the outside, are found in strongly and weakly electric fish. They are typically used for the passive electrolocation of prey and predators, but involved in locating conspecifics in electric rays, skates and catfish. Tuberous receptors are not open to the outside but covered by an epithelial cell plug and tuned to the high-frequency components of a species’ EOD. They are unique to mormyriforms and gymnotiforms, where they have evolved independently. Mormyriforms possess two types of tuberous receptor – Knollenorgans are employed in communication and mormyromasts in active electrolocation. In gymnotiforms, one tuberous receptor type is specialised for detecting the amplitude of a stimulus and another for timing, but both are used for electrolocation as well as communication.
The electroreceptors are innervated by the lateral line nerve, which relays the information to the hugely enlarged electrosensory lateral line lobe (ELL) in the medulla. This brain region is subdivided into four compartments that are specialised for detecting different components of the electrosensory input. The ELL also receives information about the timing of the EOD that is associated with the EO motor command.
Functions of electric discharges
For strongly electric fish, the function of their powerful discharges usually consists in the stunning of prey or defence against predators, but this is impossible with weak electric discharges. So why do mormyriforms and gymnotiforms live in an electrical world? Although they have been studied for some time, with studies initiated by the pioneer work of Lissman, the complexity and sophistication of the sensory world of these fish is still not completely explored or understood. Whilst they do possess eyes, they are typically either nocturnal or live in murky waters, where the use of vision is limited. Similar to electroreceptive animals that are not electrogenic, electric fish can use the perception of electric currents to detect prey and navigate around inanimate objects, but as their electric sense is active rather than passive, they are capable of more. Electrogenesis in combination with electroreception allows for the active electrolocation of objects in the surroundings (as these objects create distortions in the self-generated electric field) and sophisticated electrocommunication (as EODs differ between species, sexes and often even individuals). Both functions have evolved separately in mormyriforms and gymnotiforms and could explain why EOs with weak discharges (which have been hypothesised to represent an intermediate stage in the evolution of more powerful EOs) were retained.
Jamming avoidance response
Another striking feature of the mormyriform-gymnotiform convergence is the independent evolution of the so-called jamming avoidance response (JAR) in both groups. If signals from adjacent fish threaten to cancel each other out, pulse-type species modify the timing of the their electric discharge, while wave-type species rapidly shift the frequency of the signal. Thus, they avoid jamming of their electroreceptive system and sensory confusion. The JAR is complex and fantastically sensitive, but more remarkable is that the neural computational mechanisms and behavioural responses are nearly identical in mormyriforms and gymnotiforms. There are also interesting parallels to other animals that employ JAR, notably the bats.
Whilst the JAR in weakly electric fish is generally regarded as “helpful”, members of at least one gymnotiform species seem to intentionally jam competitors with a higher EOD frequency. Males of the brown ghost knifefish (Apteronotus leptorhynchus) are territorial and establish a dominance hierarchy, with the largest individuals having the highest EOD frequencies. Behavioural observations have shown that, rather than performing a JAR, they elevate their frequencies within jamming range of rivals during aggressive encounters (females showed a similar behaviour, although for them the relationship between EOD frequency and size or dominance is less clear). This is reminiscent of tree frogs in the genus Smilisca and cicadas in the genus Magicada, where males change their courtship calls in such a way that they overlap with those of rivals.
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Map of Life - "Electric fish: insights into convergence"
December 13, 2018