Electric fish
ASCAP May 1994, 8-11 Vol
7
In our theorising about the evolution of mood
disorders (1), we have suggested that mania and depression are exaggerations of
alternative involuntary agonistic strategies:
an escalating strategy which we have called the involuntary dominant
strategy (IDS) and a de-escalating strategy which we have called the
involuntary subordinate strategy (ISS); and that the choice of strategy
depends on the self/other comparison of relative resource-holding potential
(RHP). We have pointed out that this new
approach of regarding behavioural variation in terms of sets of alternative
strategies is something which has been developed in zoology and lends itself to
an evolutionary approach. We have
examined some examples of strategy sets in animals in order to clarify the
model (ASCAP, Nov '92 and April '93).
Here I would like to examine another example (2), which is not only a
choice between two mutually incompatible alternative strategies, but one in
which the choice depends on a self/other comparison. Therefore, although the behaviour concerned
(the emission of electric discharges) is one which has not evolved at all in
mammals, in formal terms the strategy choice is similar to the one we are
interested in, and might repay study.
Also, it is the only strategy choice which has been followed in the
brain by neuroanatomical study from the stage at
which the need for a strategy choice is detected to the final making of the
choice.
It is
thought that all ancestral fishes were electrosensitive,
using ampullary organs in the skin to detect
geological electric fields for purposes of navigation and biological electric
fields for purposes of prey detection.
This capacity has been retained by most present-day cartilaginous fish,
but was lost during the evolution of the bony fishes (our ancestors). However, electroreception
was regained independently in two lineages of bony fish; and this retrieval of the old capacity
to detect electrical fields was associated with the development of the capacity
for "weak" electrogenesis, in which
electric organ discharges (EODs) are emitted from the
muscles in the caudal half of the body and the resulting electric fields are
detected by newly evolved tuberous receptors covering the whole body
surface. The distortion of the electric
field by objects whose impedance differs from the surrounding water allows the
fish to "see" these objects, in the way that bats can "see"
by echolocation. In this way they are
able to navigate through murky water and at night, and to go to depths at which
sunlight does not penetrate. They can
also use their EODs to communicate with
conspecifics. However, the
emission of EODs by conspecifics leads to the
possibility of "jamming" if the frequencies of two fish are very
similar, because the electroreception process depends
on the detection of small differences in frequency and amplitude in particular
patterns across the body of the fish.
This difficulty has favoured the evolution of the jamming avoidance
response (JAR) in at least one branch of both lineages. When a fish detects another fish of very
similar frequency, it chooses between two mutually incompatible alternative
strategies: it either increases its own
frequency or it reduces its own frequency.
If we
describe our ranking theory in terms of resource-holding potential (RHP), we
get a very similar situation. Imagine an
agonic social group, one in which symmetrical relationships are not tolerated,
as exists in olive baboons and a large number of macaque species. In such groups there is an intolerance of
equal RHP, just as in the fish there is an intolerance of equal
frequencies. Each baboon struts around
emitting signals of absolute RHP; if he meets another baboon signalling
clearly higher RHP, he adopts the subordinate basic plan; if he meets a baboon signalling clearly lower
RHP, he adopts the dominant basic plan.
But if he meets a baboon signalling the same RHP as his own, he cannot
adopt either of his customary basic plans, and he has a problem. Or, rather, both baboons have a problem. They have to find some way of developing a
difference in RHP, or of detecting and subsequently being able to recognise a
difference in RHP. Each has the capacity
to alter his own RHP either up or down (or it might be more correct to say that
he can alter his own perception of his own RHP up or down - what Hartung (3) has called "deceiving up" and
"deceiving down"). We would
say that each has a choice of either an escalating or a de-escalating
strategy. Each of the pair of equal RHP
baboons has an interest in getting the matter settled one way or the other, and
also an interest in having it settled in a particular way; i.e., with himself as top baboon. They are in a non-zero sum game, and the
choice of strategies has been the subject of much research by game theorists -
in fact the concept of RHP was developed by a game theorist (Geoffrey Parker)
while tackling just this sort of problem.
We can assume that the same problems face a pair of electric fish which
happen to have very similar frequencies.
They both want to develop a difference in their frequencies, and it may
well be that each would prefer to adopt one strategy, such as lowering its
frequency, which may involve less energy expenditure than raising its
frequency. Each would therefore like the
other fish to immediately raise its frequency - and while both are waiting for
the other to do so, both are paying the cost of having incapacitated navigation
systems.
What
the fish do is to examine the frequencies and work out whether their own is
slightly higher or slightly lower (they can tell which frequency is emanating
from themselves). If theirs is slightly
lower, they then lower their frequency further, and vice versa. Presumably they have some plan in the event
of the frequencies being exactly the same - some sort of default setting which
says, for instance, "if no detectable difference, raise
frequency". In the case of baboons
evaluating each other's RHP, much the same process seems to be taking
place. They explore each other's RHP,
using species specific signals (ritualised fighting) which take the form of
statements of equal or superior (favourable) relative RHP. When the baboon threatens the other, he is
saying "My RHP is greater than yours" and when the other baboon threatens
back, it is saying, "No, it isn't".
Eventually one baboon decides that its RHP is very slightly lower than
the other's, and it then adopts the de-escalation strategy which consists, at
least in part, of a lowering of its RHP.
In this way a difference in RHP is created where none (or at least no
clearly detectable difference) existed before.
It may
be instructive to look at the similarities and differences between the
situations of the baboons and the fish.
Similarities
There is a population whose well-being depends
on all the members having different values of some variable X.
If two members happen to have the same value of
X, each can deal with the problem by raising its value of X or by lowering its
value of X.
It is in both their interests to create a
difference, but their interests conflict over which
increases X and which lowers it.
Satisfactory outcomes occur if:
1. One makes an adjustment and the other does
nothing.
2. Both make adjustments but in opposite
directions.
An unsatisfactory outcome occurs if both make
adjustments in the same direction.
They examine the values of X to see if there is
a slight difference. If they find a
difference, they adopt a strategy which enlarges the difference. If there is no detectable difference, they
could randomise the choice of strategy, or they could implement a default
strategy which could be either to raise or to lower X. In the latter case the population would be
dimorphic, but the morphs would only be apparent when the comparison process
was activated, and even then an observer could not know whether a default
setting had been activated, or whether a minute difference had been
detected. The default strategy could be
either genetically determined or it could be contingent on some environmental
factor, active either earlier in life or concurrently with the strategy
choice. Or it could be randomised. Or it could be a combination. For instance, there could be a genetically
determined strategy which read, "if your first social encounter was with
an individual of lower X than yourself, activate a default setting of
"lower X" if you are feeling hungry, but "raise X" if you
have eaten recently;
if your first encounter was with an individual of higher X,
operate a randomised default strategy, with a frequency of "raise X"
of 0.3". In the case of RHP, I
think that a default setting of "raise RHP" is what Maynard Smith
refers to as a "hawk strategy" and "lower RHP" is what he
calls a "dove strategy" (4).
Differences
The baboons explore the difference in RHP by
exchanging signals, which are at the same time statements of favourable
relative RHP (the fact that the signal is given) and of absolute RHP (the
intensity of the signal). We have
defined signals of favourable relative RHP (catathetic
signals) as signals which lower RHP in the receiver, provided they are not
returned in full measure. It is the
detection of the fact that it is not returning the adversary's catathetic signals in full measure which convinces the
baboon that it is losing the fight and leads to it adopting the de-escalating
strategy. Therefore in the case of the
baboon, it does not matter whether we say that RHP is lowered by the catathetic signals of the adversary, or as part of its own
de-escalating strategy. The two things
are part of a systemic dyadic interaction which is recursive in its causative
mechanisms.
Likewise, with a pair of baboons it does not matter whether we say that
one baboon lowers its RHP or that both baboons look at the RHP scale with much
higher definition, and see differences which were previously
sub-threshold. However, if we are
dealing with a group, the distinction does matter, because in lowering its RHP
to create a difference with baboon A, a baboon may alter its RHP difference
with previously lower-ranking baboons, either becoming equal in RHP or even
lower than those to whom it was formerly superior. This last situation seems to be the case in
many animal species, as a defeated animal may fall to the very bottom of the
social hierarchy.
The comparison of frequencies
The most simple thing would be for the fish to
compare the incoming jamming frequency with an "output copy" of its
own frequency; and,
if the income frequency was higher, to lower its own frequency, and vice
versa. But they do not do this. They do not appear to have evolved the
capacity to retain an output copy. They
can tell from the pattern made by the two frequencies on their bodies whether
the incoming frequency is higher or lower than their own. Then they alter their own frequency
accordingly.
We do
not know how animals (or humans) make comparisons of relative RHP. Probably when the capacity to make the
comparison first evolved it was based on a single feature like size, although
even this comparison cannot have been easy because the representation of one's
idea of one's own size, and one's idea of the size of an adversary, use
different kinds of information. It is
not as simple as comparing two shades of wall-paper placed side by side. At some stage we should make models of the
comparison which give different predictions, but at this stage I think it helps
just to know that this kind of self/other comparison is made in electric fish, and that the result of the comparison decides between
alternative strategies.
References
1.
Price, J.S., Sloman, L.,
2. Heiligenberg, W.F. (1991) Neural Nets in Electric Fish.
3. Hartung, J. (1987) Deceiving down: Conjectures on the
management of subordinate status. In J. Lockard and
D. Pulhus (Eds) Self-deceit: an Adaptive Strategy.
4.
Maynard Smith, J. Evolution and the Theory of Games.
14.4.94
jp\aa\fish.2
these weak discharges of
less than 10 volts can be compared to the electric eels and rays which use
electrical discharges of up to 600 volts to stun and kill their prey - the weak
discharges are used for locating prey and other objects, and for communication
with conspecifics).
They
can distinguish between impedance due to capacitance and that due to
resistance, so they can sense at least one quality of objects as well as size,
shape and direction, in much the same way that we see colour. The frequency of the EODs
ranges from a few cycles per second to 1,800 Hz. The fish can detect amplitude modulation of
as little as 1%. They can detect phase
modulation (the difference in timing of the pulses at two points on the body
surface) of a fraction of a millisecond;
this compares with the owl threshold of several milliseconds (in the
fish, whereas the synapse between receptor cell and afferent nerve is
chemically mediated, all the interneuronal synapses
are electrically mediated, whereas in the owl all synapses are chemically
mediated, and the greater rapidity of electrical transmission is thought to
account for the greater power of phase detection in the fish).
The jamming avoidance response
However, the emission of EODs
by conspecifics leads to the possibility of "jamming" if the
frequencies of two fish are very similar, because the electrodetection
process depends on the summation of small differences in phase and amplitude in
repeated pulses in particular patterns across the body of the fish. Coincidence in a single pulse does not
matter, because that information can be discarded; but coincidence in a whole series of
pulses scrambles the usual location information. This difficulty has favoured the evolution of
the jamming avoidance response (JAR).
When a fish detects another fish of very similar frequency, it chooses
between two mutually incompatible alternative strategies: it either increases its own frequency or it
reduces its own frequency.
ASCAP June 1995, p 10-13
Electric fish:
a harmonious model for asymmetrical relationships
When I recently wrote to Ascap about electric fish, and later about
authoritarian personality, I little thought that I would soon be sitting down
and writing about authoritarian personality in electric fish. And yet, having got more fish material from
the library (1), that is what I find myself
doing. Let me start with some general
information about the evolution of electric fish.
Evolution of electro-receptivity
It is thought that electro-receptivity evolved
several times and shows parallel evolution.
Most cartilaginous fishes are electroreceptive. Only two lineages of bony fishes
are, and they are the African mormorids and the South
American gymnotiforms, both being freshwater fish and
therefore likely to very distant relations.
Evidence from the receptor organs and brain nuclei suggests that these
three lineages developed the capacity independently, but in each case from the
tissues of the lateral line system.
They
all have ampullary organs which are used to detect
external electric fields (such as those given off by prey), and the fields
created when the fish moves in relation to the earth's magnetic field. Only the bony fish have tuberous organs which
are used to receive their own electric organ discharges (EODs)
and those of conspecifics, and these are adapted to receive only the
frequencies that it has been adaptive for them to receive during evolution.
Evolution of electrogenesis
The capacity to create electric fields in the
surrounding water is also thought to have evolved several times. Bullock (2) says, (p. 670) "...it
appears most likely that electric organs were invented repeatedly,
independently, in species already possessed of electroreception,
in unrelated orders of elasmobranch and teleost. Only in one
case, the stargazers (Uranoscopidae), is it doubtful
whether electroreception coexists with the electric
organs.....nothing is known about electroreception in
invertebrates, reptiles or birds" [it occurs in urodele
amphibians and one mammal (the duck-billed platypus)].
There
are two distinct forms of weak EOD, wave forms and pulse forms, and both occur
in both African and American families.
Strong EODs are used for stunning and killing
prey, and for defence, and they occur in the torpedines. The weak EODs are
used for navigation and communication.
The receptors detect alterations in impedance in the electric field, and
they can distinguish whether such alterations are due to capacitance or
resistance, so these fish have the capacity for "seeing' an environment
which would be very strange to us.
The
electric organs are evolved from striated muscle (which has lost the capacity
for contraction). Therefore the
discharges can be abolished with curare (very useful in experimentation). Larvae also have electric organs, which may
or may not be homologous with the adult forms.
Most organs are developed from trunk musculature and are innervated by
spinal electromotoneurones, but some are developed
from the extraocular muscles and innervated by
cranial nerves. Some fish have accessory
electric organs which may discharge at a different rate from the main
organ. One group (Apteronotidae)
has a "neurogenic" organ developed from
spinal motor nerves (probably from the nerves which innervate its larval myogenic organ) and this can reach a frequency of 1,700
cycles per second (and of course it is not affected by curare). One fish has an electric organ developed from
sensory nerves.
Sex differences in frequency
In wave form species (which emit an almost
sinusoidal wave of alternating current) the frequency of the discharge is the
most important information. There is a
tonic or background frequency which is used for species, sex and possibly
individual recognition. This is given
off 24 hours a day, so the electric fish is par excellence an individual
who "cannot not communicate". In some species, the frequencies of the two
sexes differ but overlap, in most cases the male has a lower frequency, but in
a few species the female has a lower frequency.
It is interesting that when the males have a lower average frequency,
the male will only mate with a female having a higher frequency, even though
many of the females it meets have a lower frequency.
Wave form and sex hormones
In many species the wave form of females
differs from that of males, and this is due to the nature of the electrocytes in the electric organ, and to their arrangement
and their number. In most of these cases
the female wave form can be converted to the male form by androgens (by
changing the electrocytes into male form) and in
these cases the electrocyte is a target tissue for
androgens like the syrinx of songbirds and the penile
bone of the rat (2). Wave forms which do
not differ between the sexes are not affected by androgens. In some cases when males are kept in
captivity, their EOD wave forms alter to the female type, and this may reflect
a change in sex, since we know that sex in fish is often socially determined.
Frequency modulation and agonistic behaviour
Modulation of the tonic frequency is used in
both reproductive and agonistic behaviour. Short interruptions in the tonic
discharge (< 1 second) are used as threat displays and courtship displays; they may cause
rivals and subordinates to flee. Long
interruptions (> 1 second, extending to total electrical silence) serve as
submissive displays, and reduce attack by rivals and dominants. These conventions apply to both pulse and
wave forms of both mormyrids and gymnotiforms,
in fact to all electric fish except the Apteronotids
(which have the neurogenic electric organ) and so
represent a remarkable case of parallel evolution.
Short
increases in frequency (< 1 second) of 10 to 50 Hz also act as threat
signals, while long rises (5 to 40 seconds) of 2 to 20 Hz signify
submission. It is not known how the
significance of rises differs from that of interruptions. Other threat signals in electric fish are antiparallel swimming and head butting.
Frequency and social rank
In those species of electric fish which form
social hierarchies, frequency also varies with dominance. In some species the dominant fish has a
higher frequency, in some species lower.
In the latter, if a fish becomes dominant, its frequency becomes
lower. In some species in which dominant
males have lower frequencies than other males, dominant females have higher
frequencies than other females.
When
two fish of the same species are paired together, they tend to develop
frequencies which differ by exactly an octave (1, p. 514). So far this has only been reported for
opposite sexed pairs, so it is not known whether it is a reflection of
dominance relations or pair bonding. Nor
is it known how the regulation is achieved.
However, the formal similarity to the adjustment of RHP in complementary
marital relationships is striking (3):
What seems more likely, from what we know
clinically, is that the "one- up" husband (or wife) tries to keep his
spouse's exercise of control [RHP] a constant amount below his own exercise of
control [RHP]. What is maintained homeostatically is not the absolute level of control but
the difference in
control between husband and wife, what might be called the "control
gap" [RHP gap).
More generally, the "one-up" spouse maintains a gap on what
Birtchnell (1987) has called the "vertical dimension" which describes
a number of correlated variables such as mood, rank, self-esteem,
self-confidence, dominance, and, in the last resort, the capacity to define the
relationship rather than accept the definition provided by the other. Colloquially, we might say he tries to
maintain a constant level of "one-upness"; more
technically he tries to maintain a constant vertical-gap setting between
what he feels to be his own position on the vertical dimension and what he
perceives his wife's to be. This
"gap" model has the advantage of embracing the phenomena of
redirected aggression;
if the husband's mood is lowered after receiving punishment from
his boss at work, he restores the vertical gap at home by putting his wife down
(or omitting to boost her). The feedback
loop is probably below conscious awareness:
even though he may be aware that he is putting his wife down, he does
not understand why he is doing it; and
many signals intended as boosting signals are received as putting-down signals,
especially in the case of "constructive" criticism (MacLean, 1976).
I am not sure how many situations there are in
which one vertebrate compares itself with a conspecific, and then makes a decision which depends on the comparison. There is the comparison of RHP which
determines the decision whether to attack of flee in agonistic behaviour, and
this is widespread among vertebrates.
Then there are these two instances in electric fish, the jamming
avoidance response which I discussed last time, and this pair-bonding
situation, in which a fish either selects another with a complementary frequency,
or creates a desired frequency gap by altering its own or its partner's
frequency. And there is mate selection
in the herring gull, which, substituting size for frequency, is similar to mate
selection in the electric fish.
Tinbergen (4) observed in herring gulls that, although the range of
sizes of male and female overlapped considerably, he never observed a mated
pair in which the female was larger than the male. This means that the gulls must compare their
sizes during courtship, and desist if the female is larger than the male.
Is
there a basic vertebrate plan for self-other comparisons, which has been drawn
on for all these four, and possibly other, comparisons? Or did the self/other comparison evolve
separately in each situation? We can do
no more than speculate. In the case of
RHP and size in gulls, there could well be a common comparison process, as the
RHP comparison may well have started off as a simple size comparison. But it is less likely with the electric fish,
in which the whole plan for electrogenesis and
communication by electric fields evolved independently (our own ancestors are
thought to have been electroreceptive but not to have
had electrogenetic powers). It is more likely that the capacity for
self-other comparison evolved as part of this new system, rather than that an
existing self/other comparison system was brought in from somewhere else in the
brain, rather as someone developing an aeroplane might have used an engine
designed for powering a car.
Of
course RHP does not work like the harmonic scale, so there is no obvious size
of RHP gap to match the octave of frequency gap. In fact, the variability of RHP gap is
probably important, in that it is likely to vary with the
"insecurity" of the dominant authoritarian partner. The more secure he feels, the less gap he needs.
Therapeutically, this means that one can aim at reducing the gap, short
of achieving total symmetry. One could
not do this with electric fish, because the system
would tend to return the gap to the octave (perhaps one could reduce a gap from
two octaves to one octave!). Means of
reducing the RHP gap involve educating the dominant partner that gap reduction
brings benefits rather than costs: his
more powerful wife will use her power to further his interests rather than her
own competing interests;
a more sociable wife will use her capacity to cultivate his
friends rather than fill the house with her own; a more highly sexed wife will increasingly
satisfy him rather than give her favours to others (etc., etc.).
For
completeness, to the above one must add two categories of self/other comparison
with which we are very familiar in humans.
There is comparison of what Paul Gilbert has called social
attention-holding power (SAHP), in which the comparison asks the question,
"am I more attractive than he/she?" in the hedonic competition for
prestige. And there is the group
membership comparison which asks the question, "Is he/she the same as me?". This latter
comparison occurs in insects and rodents in which groups of the same species
differ in smell.
Insensitivity of brain to electric fields
It has been suggested that the human brain
might be sensitive to electric fields.
But to me, to envisage this possibility persuades exactly the opposite,
and emphasises how very insensitive the human brain is to either direct or
alternating electric fields. Humans by
now must have been exposed to a fantastic variety of fields, including a range
of frequencies of alternating current that must include the capacity of any
imaginable receptor systems. And yet no
behavioural changes have been produced.
It seems as if the brain were specifically protected from electrical
disturbance. Look at the difficulty we
have in inducing seizures in giving ECT.
Lightning affects the body but not the mind. It looks as though electroreception
has been thoroughly bred out of our systems, possibly because those of our
ancestors who remained electrosensitive were at some
disadvantage, possibly from the electric discharges of some predatorial
dinosaur.
Possibly we did this by evolving chemical neurotransmission, which seems
otherwise to be an extraordinarily cumbersome addition to a system which is
based on purely electrical transmission.
But in requiring chemicals for nerve to nerve transmission we made
ourselves invulnerable to outside electrostimulation,
and myelin did the rest.
References
1.
Hopkins CD (1988) Neuroethology of electric communication. Ann Rev Neurosci 11, 497-535.
2.
Bullock TH (1986) Significance of findings on electroreception
for general neurobiology. In Electroreception ed TH Bullock & W Heiligenberg.
3.
Price, J.S. (1991) Homeostasis or change? A systems theory approach
to depression. British Journal
of Medical Psychology, 64, 331-344.
4.
Tinbergen, N. (1953) The Herring Gull's World.
sent to Russ 16.6.94