Download The Elementary Nervous System Revisited1

AMER. ZOOL., 30:907-920 (1990)
The Elementary Nervous System Revisited1
G. O. MACKIE
Biology Department, University of Victoria,
Victoria, British Columbia, V8W 2Y2, Canada
SYNOPSIS. Parker's theory of the origin of the nervous system is discussed along with
later interpretations. Attention today has shifted from the cellular to the molecular level,
and it has become clear that many of the molecules and mechanisms thought of as typically
neuronal have homologs or counterparts in non-nervous cells and unicellular organisms.
This applies to signalling chemicals, receptors, second messenger systems and ion channels,
and also to the production of electrical events. Parker's view of sponges as a group lacking
nerves but possessing independent effectors is still acceptable, but some sponges (and also
higher animals) employ non-nervous signalling pathways to coordinate their effectors.
Thus, nerves are not always necessary for coordinated behavior. Cnidarians like hydra
have seemingly simple, two-dimensional nervous systems with little or no centralization,
but even such systems can be surprisingly complex, and the more advanced cnidarians
show neurophysiological specializations as sophisticated as those of many higher invertebrates. Examples of ingenious cnidarian solutions to behavioral problems are given. No
existing animals have "elementary" nervous systems if that term implies the existence of
crude or inefficient functional adaptations.
Where did nerves come from? Parker
derives
them from specialized receptive
It is now seventy years since the publiepithelial
cells in an outer body layer in
cation of The Elementary Nervous System in
which G. H. Parker (1919) summarized which muscle cells had already developed.
views he had been developing over the pre- These primitive receptive cells became
vious decade and would continue to hold neuro-sensory cells and provided a means
with little change until the end of his career for exciting the muscles locally, but they
(Parker, 1946). The book presents a syn- also developed processes by which they
thesis and critique of ideas and experi- communicated with one another, forming
ments relating chiefly to the origin of the a nerve net capable of spreading excitation
nervous system and its organization in coel- over whole muscle fields much as we see
enterates. Parker proposed that the ner- in present-day cnidarians. In Parker's time
vous system arose because of the need to it was thought that cnidarian nerve nets
coordinate "independent effectors," in were syncytia, so by implication the first
particular primitive contractile cells such nerve nets to evolve would also have been
as those of sponges, where there are as yet syncytia and the development of synaptino nerves. Muscles were the most obvious cally connected neuronal arrays would have
"nucleus" around which the nervous sys- been a later development. We now know
tem formed. Later, the nervous system that cnidarian neurons can be intercon"appropriated" other effectors, though a nected by chemical synapses, gap junctions
few remained independent (ciliated cells, or syncytial cytoplasmic bridges. There is
no particular reason for supposing the synchromatophores, cnidocytes).2
cytial condition to be primitive. Although
INTRODUCTION
' From the Plenary Session on Organismal Systems:
Animals and Behavior presented at the Centennial
Meeting of the American Society of Zoologists, 2730 December 1989, at Boston, Massachusetts.
2
Transmission of metachronal waves in ciliated *:pithelia does not involve the nervous system, though
arrests and reversals result from depolarization by
nerves (see Aiello, 1974). Chromatophores in siphonophores and ctenophores appear to be true independent effectors (see Mackie el al., 1987). Cnidocytes
are sometimes innervated, and their response thresh-
olds might therefore be affected by nervous input,
but this has not been proved. Some are not innervated
at all. Others are subject to threshold modifications
relayed to them from adjacent epithelial chemoreceptors (Watson and Hessinger, 1989; see also Thorington and Hessinger, 1988). As Horridge (19686)
notes, "probably every cell in every animal can be
regarded as an independent effector in that it makes
some response at some time to stimulation which is
not via a controlling neuron."
907
908
G. O. MACKIE
nearly all the fields touched upon by Parker have been radically transformed since
1919, his theory in broad outline can still
hold place alongside other explanations of
how nerves evolved. For the most part,
these later explanations have been
prompted by advances in understanding of
physiological processes such as cell communication, pattern generation and neurosecretion.
Pantin (1956), whose researches on sea
anemones provided strong evidence that
like higher animals cnidarians had synaptically interconnected nervous systems in
which facilitation could occur at the junctions, argued that nervous systems did not
evolve on the basis of single cells, but of
whole networks innervating multicellular
motor units; they functioned from the
beginning to coordinate the behavior of
the whole animal. Like Parker, Pantin left
the way open for primitive, non-nervous
("neuroid") conduction systems which
arose before the evolution of the nervous
system and survived and coexisted with
nerves after the latter had evolved.
The ability to generate activity endogenously is as much a part of the definition
of a nervous system as is the ability to
respond to stimulation, and the cnidarian
nervous system is no exception, as Passano
(1963) made clear. His work on hydra and
syphomedusae revealed abundant evidence of complex rhythmic activity involving multiple, interacting pacemakers. He
saw the nervous system as evolving from
specialized pacemaker cells whose function
was to generate contractions within groups
of protomyocytes. These pacemaker cells
would have become neurons, retaining
rhythm generation as their primary function, and only later becoming specialized
for conduction over long distances and as
sensory receptors.
Passano and I working later in the sixties
discovered that hydromedusae and siphonophores have excitable epithelia which
conduct action potentials and serve as
pathways mediating certain types of behavior, sometimes in collaboration with the
nervous system, sometimes on their own.
These "neuroid" impulses were assumed
to propagate through low-resistance path-
ways between the epithelial cells. (Later,
electrical and dye-coupling were demonstrated and the pathways were identified
as gap junctions.) These and similar findings prompted Horridge (1968a) and
Mackie (1970) to propose that nerves
evolved from tissues whose cells were
already connected by pathways serving for
metabolic exchange and electrical current
flow, making cell to cell propagation of
action potentials possible. Nerves, with
their elongated form and functional isolation from surrounding tissues, would have
arisen in response to a need for a more
selective type of excitation in which effector sub-groups could be controlled independently.
In all these theories it is the electrical
properties of nerves or their precursors
(receptivity, production of local or propagated potentials, pacemaking) that are seen
as the principal forces driving selection in
neuronal evolution. Other theories favour
the secretory role. According to Grundfest
(1959,1965) the ancestral neuron may have
been a secretory cell that developed a conducting segment in between its receptive
and secretory poles. Horridge (19686),
refining his earlier position, suggested that
neurons first appeared as neurosecretory
or growth regulatory cells. Only later did
their elongated processes come to serve for
impulse propagation. Lentz (1968) also
stressed the humoral and trophic aspects
of nerves but regarded these as having
evolved concurrently with electrical transmission in the general context of effector
control. The idea that receptive, electrogenie and neurosecretory functions coevolved in primitive protoneurons received
a boost when electron microscopy showed
that nerve cells in hydra not only have
receptor poles with a sensory cilium, and
basal neurites making synaptic contact with
effectors but they also contain neurosecretory material (Westfall, 1973; Westfall and
Kinnamon, 1978; see further Lesh-Laurie,
1988).
It often seems to be assumed that new
tissue types arise gradually, rather like new
species, by steady accumulation of small
changes, eventually becoming distinct from
other tissue types. As Buss (1987) suggests,
ELEMENTARY NERVOUS SYSTEM
emergent cell lines may have competed
amongst themselves, some becoming
established simply by virtue of their higher
replication rates, without necessarily benefitting the organism in the first instance.3
What was not clear in Parker's time was
that all the cells in the body have the same
genes. They differ only in which genes they
express and when. Mutations making possible the emergence of nerves would have
been available to all the cells in the body,
not just to those in the pre-neuronal lineage, and vice versa. The process is therefore not at all like the origin of species.
Given suitable conditions, non-nervous cells
can express genes we think of as being typically neuronal. Thus, vertebrate oocytes
express receptors for acetylcholine, GABA
and epinephrine (see Carr, 1990) and voltage-gated channels and neuropeptides are
found in various non-nervous cells. Since
Parker's day, then, the distinction between
neurones and non-nervous cells has become
somewhat blurred4 and it now seems most
appropriate to ask not which cell lineages
originally gave rise to nerves but where the
genes expressed in neurogenesis originally
came from. This does not invalidate the
kind of question Parker was asking, but
transfers the focus of attention to a more
fundamental organizational level.
PROPHETIC MOLECULES IN PROTISTS
Haldane (1954) proposed that signalling
by means of neurotransmitters and hormones had its origin in chemical signalling
in Protozoa, and he gave examples of ciliate mating types where conjugation is controlled by such signals. Interestingly,
3
Neurons of course are postmitotic, so it would
have been neuroblasts which did the competing in
neural evolution. For Buss's mechanism to work, it
must be assumed that the critical changes in the preneuronal stock were heritable. This would not have
been a problem if nerves evolved in a hydra-like ancestor, as the interstitial cells which act as neuroblasts in
hydra also give rise to the gametes.
4
The participants at a recent meeting on neuronal
evolution attempted unsuccessfully to compile a list
of characters by which neurons could be denned (see
Anderson, 1990, closing remarks). Either the "diagnostic" features are not present in all neurons, or they
are found in some non-nervous tissues as well as in
909
therefore, a mating pheromone in Blepharisma proves to resemble serotonin (Miyake,
1984). Various ciliates have receptors for
acetylcholine, catecholamines and other
neuroactive substances (see Carr et al.,
1989). The a-type mating factor of yeast
shows sequence similarities with the vertebrate reproductive hormone GnRH and
mimics its effects, stimulating release of
luteinizing hormone from pituitary cells
(Loumaye et al., 1982). Both are produced
by post-translational cleavage of a pro-protein. Whether or not there is any true
homology here is unclear, but the example
is interesting because it shows peptides
being used for behavioral signalling at the
unicellular level.
Tetrahymena produces ^-endorphin and
shows positive chemotaxis in a gradient of
this opiate. It has recently been shown to
possess a 110 kDa membrane protein
closely resembling annelid and vertebrate
opiate receptors. Chemotaxis is blocked by
naloxone, like opiate-mediated responses
in mammals (Zipser et al., 1988).
Though cAMP functions as an internal
messenger in neurotransmitter receptor
systems in higher organisms, the same molecule, manufactured through the same
synthetic pathway, serves as an external
chemical signal or pheromone in Dictyostelium. The slime mold cAMP receptor
appears to belong to the same molecular
family as the /Sadrenergic and muscarinic
acetylcholine receptors of mammals: all of
them have seven trans-membrane-spanning segments, with the amino terminal on
the outside and the carboxy terminal on
the inside. Furthermore, the G-proteins
involved in signal transduction in these
cases appear homologous (see Devreotes,
1989). While these similarities could all
have arisen by convergence, it seems easier
to suppose that at least some of the genes
concerned arose in unicellular organisms
and were inherited and modified by metazoans, while others may have arisen independently (van Houten, 1990).
In early metazoans transmitter receptors
might have evolved in relation to the binding of external signalling molecules
mediating substrate recognition. This is
suggested by the observation that inver-
910
G. O. MACKIE
tebrate larval metamorphosis and settlement can often be induced by chemicals
emanating from the preferred substrate.
Several neuroactive compounds trigger
metamorphosis, e.g., GAB A in the case of
abalone larvae. GABA-mimetic compounds occur in the red algae on which the
larvae settle (Morse, 1985; see further Carr
etal, 1989).
Ion channels, "the quintessential nervous molecules" (Kung, 1990), are found
in bacteria, yeasts and protozoa (see Saimi
et al., 1988). Two sorts of channel have
been found in Escherichia coli, one of which
is mechanically gated and the other voltage
gated. Perhaps the very first channels to
evolve were stretch-sensitive channels
serving as osmotic stress sensors. Mechanoand voltage sensitive channels, one of them
selective for K+, have also been found in
yeast cells. Paramecium may have as many
as nine distinct, ion-selective membrane
channels, including voltage-, calcium- and
mechanically gated varieties (see Kung,
1990), while Stylonychia has at least seven
(see Machemer and Deitmer, 1987). Many
of these channels appear to correspond to
well-known channels in higher animals.
Whereas Ca++ and K+ channels are found
everywhere "from Paramecium to poultry"
(Hille, 1984), Na+ channels do not appear
until the metazoa,5 and on their "first
appearance" in Cnidaria, they are not
tetrodotoxin-sensitive; however, most or
all voltage-gated channels appear to be
descended from a common ancestral molecule (Catterall, 1988). Hille (1984) suggests that oubain-sensitive Na+-K+ ATPase
(sodium pump) molecules evolved coincidentally with Na+ channels.
and back ends and in the ciliary membranes.
Paramecium and other ciliates can be
regarded as "free swimming sensory cells"
as they respond to a variety of environmental stimuli (mechanical, thermal,
chemical, photic, ionic) by changing their
membrane potential. However, they also
respond behaviorally, changing shape or
altering the pattern of ciliary beating in
their capacity as free-swimming effectors.
Some of the most basic protozoan effector
systems must have been available to early
metazoans for use with only minor modification. Contractions in ciliates are typically due to spasmins (not present in metazoans) but actin and myosins I and II are
present in sarcodine and slime mold amoebae {e.g., Fukui et al., 1989), and would
almost certainly have been present in early
metazoan cells as the starting point for
muscle evolution. Long before muscles
evolved, these molecules were probably
serving the cause of motility. Actin seems
to be universally present in animal and plant
cells, and is responsible for such fundamental motile processes as cell locomotion,
neuronal growth cone extension and cytokinesis (see Bray and White, 1988). Ciliary
movement works in similar ways in protozoans and metazoans, being based on
tubulin-dynein interactions, with metachronal waves propagated mechanically (or
at least by a process that does not involve
transmembrane potential changes) while
arrests and reversals are brought about by
ion fluxes through membrane channels.
EARLY ELECTROGENESIS
Several writers (for instance Bishop,
As Deitmer (1988) points out, ciliates 1956, and Pantin, 1956) have suggested
resemble neurons not only in their posses- that graded, locally spreading electrical
sion of multiple ion channels, but in the potentials are evolutionarily more primifact that the channels are not distributed tive than propagated action potentials, and
uniformly over the cell surface. Some neu- that early nerves may have operated withrons are known to have distinct channel out action potentials. To spread signals for
populations in dendrites, soma, axon and any distance in this way, neurons would
presynaptic terminals, while in ciliates dif- have needed large diameters, high memferent channels may be found at the front brane resistances and/or myelin-like insulation. Certainly, local currents must have
been there from the start, as they form the
5
However, the heliozoan Actinocoryne contractilis has
a sodium-calcium action potential (Febvre-Chevalier basis for bringing the membrane up to spike
threshold. At the same time, the capacity
etal, 1986).
ELEMENTARY NERVOUS SYSTEM
911
isolated SYSTEM
from the external. Nevertheless,
for all-or-none spike propagation
probably NERVOUS
ELEMENTARY
ELEMENTARY
NERVOUS
SYSTEM
911
911
did not have to await the evolution of the mesenchyme does shelter gametes and
cellsfrom
and itthe
provides
an environment
nerves,
as it is well
developed
in many
pres- other
isolated
external.
Nevertheless,
isolated
from
the
external.
Nevertheless,
for
spike
propagation
probably
for all-or-none
all-or-none
spike
propagation
probably
in
which
electrical
and
chemical
gradients
ent-day
protozoans.
Where
in
nerves
action
and
the mesenchyme
mesenchyme does
does shelter
shelter gametes
gametes
and
did
did not
not have
have to
to await
await the
the evolution
evolution of
of the
could
in
theory
be
set
up
and
nutrients
and
potentials
are
needed
to
convey
signals
over
other cells
cells and
and itit provides
provides an
an environment
environment
nerves,
nerves, as
as itit isiswell
welldeveloped
developed in
in many
many prespres- other
diffuse
without
leaking through
long
distances,
this isWhere
not necessarily
in hormones
in
and
gradients
in which
which electrical
electrical
and chemical
chemical
gradients
ent-day
protozoans.
in
action
ent-day
protozoans.
Where
in nerves
nerves so
action
the
body
wall
excessively.
Protozoa.
It
would
apply
in
cases
such
as
could in
in theory
theory be
be set
set up
up and
and nutrients
nutrients and
and
potentials
potentials are
are needed
needed to
to convey
convey signals
signals over
over could
Noctiluca
where this
impulses
Althoughdiffuse
therewithout
are noleaking
neurons
in
through
hormones
diffuse
without
leaking
through
long
necessarily
so
long distances,
distances,
this isis not
nottriggering
necessarilybioso in
in hormones
luminescence
have
circumnavigate
are
fixed tissue pathways
the
wall
the body
bodythere
wall excessively.
excessively.
Protozoa.
apply
in
Protozoa. ItIt would
would to
apply
in cases
cases such
such aas
as sponges,
huge
central
vacuole
(Eckert,
1965),
but
in where the cells are joined by stable interNoctiluca
Noctiluca where
where impulses
impulses triggering
triggering biobioAlthough
Although there
there are
are no
no neurons
neurons in
in
Stentor
the length
constant
is large relativeaa cellular
connections.
Some
of
thesepathways
tissues
luminescence
have
to
luminescence
have
to circumnavigate
circumnavigate
sponges,
there
are
fixed
tissue
sponges,
there
are
fixed
tissue
pathways
tohuge
bodycentral
lengthvacuole
(Wood,(Eckert,
1982); as
the cyto"almost-muscles"
as they
consistinterof
1965),
but
huge
central
vacuole
(Eckert,
1965),
but in
in are
where
the
by
where
the cells
cells are
are joined
joined
by stable
stable
interplasm
is approximately
isopotential,
there actin-containing
contractile
cells.
These
Stentor
the
isis large
Stentor
the length
length constant
constant
large relative
relative
cellular
cellular connections.
connections. Some
Some of
of these
these tissues
tissues
would
seem
to be(Wood,
no need1982);
for propagation
(myocytes)
are concentrated
inconsist
sphinc-of
to
length
as
to body
body
length
(Wood,
1982);
as the
the cytocyto- cells
are
"almost-muscles"
as
they
are
"almost-muscles"
as
they
consist
along
membrane.
The
significancethere
of ter-like arrays around the osculum and poreof
plasm
isis approximately
isopotential,
plasmthe
approximately
isopotential,
there
actin-containing
actin-containing contractile
contractile cells.
cells. These
These
the
action
potential
here
must
primarily canals
in some sponges.
Parker found
that
would
seem
to
need
for
would
seem
to be
be no
no
need
forliepropagation
propagation
cells
(myocytes)
are
concentrated
in
sphinccells
(myocytes)
are
concentrated
in
sphincinalong
its capacity
for signalThe
amplification.
could
spread
for
short
the
significance
along
the membrane.
membrane.
The
significanceInof
of contractions
ter-like
pore
ter-like arrays
arraysaround
around the
the osculum
osculum and
anddispore
Stentor,
a
15-25
mV
receptor
potential
is
tances
(up
to
about
a
centimeter)
in
these
the
the action
action potential
potential here
here must
must lie
lie primarily
primarily canals
that
canals in
in some
some sponges.
sponges. Parker
Parker found
found
that
converted
into
a
65-75
mV
action
potena process
he spread
called neuroid
conin
in its
its capacity
capacity for
for signal
signal amplification.
amplification. In
In tissues,
contractions
could
for
short
discontractions
could
spread
for
short
distial,
allowing
a much
greater
calcium
influx,isis duction—"the germ from which nervous
Stentor,
aa 15-25
mV
receptor
potential
Stentor,
15-25
mV
receptor
potential
tances
(up
to
about
a
centimeter)
in
these
tances
(up
to
about
a
centimeter)
in
these
By affectenough
to induce
reversal.
has grown."
To contract,
converted
into
65-75
mV
potenconverted
into aaciliary
65-75
mV action
action
poten- transmission
tissues,
he
neuroid
contissues, aa process
process
he called
called
neuroid the
coning
all
parts
of
the
membrane
equally,
the
sphincters
had
to
be
directly
stimulated.
In
tial,
tial,allowing
allowingaamuch
much greater
greater calcium
calcium influx,
influx, duction—"the
germ
from
which
nervous
duction—"the
germ
from
which
nervous
spike
alsoto
coordinates
the
absence
of
any
evidence
of
nerves
ParBy
affectenough
induce
reversal.
Byeffecaffect- the
enough
toprecisely
induce ciliary
ciliary
reversal.
transmission
transmission has
has grown."
grown." To
To contract,
contract, the
the
tor
response
Wood,
1990). Inequally,
the early
thereforehad
treated
them
as prime
exam-In
ing
all
of
the
ing
all parts
parts(see
of the
the membrane
membrane
equally,
the ker
sphincters
to
be
directly
stimulated.
sphincters
had
to
be
directly
stimulated.
In
nervous
system,
spike coordinates
electrogenesis
of
independent
effectors.of
spike
precisely
effecspike also
also
precisely
coordinates the
themight
effec- ples
the
absence
of
any
evidence
nerves
Parthe
absence
of
any
evidence
of
nerves
Parhave
been significant
for 1990).
similarIn
tor
(see
the
tor response
response
(seeWood,
Wood,
1990).
Inreasons,
the early
early ker
still not clear
howthem
contractions
spread
It istherefore
treated
as
examker
therefore
treated
them
asprime
prime
examperhaps
in
the
context
of
secretory
or might
connervous
nervous system,
system, spike
spike electrogenesis
electrogenesis
might inples
slow, never more
sponges.
Spread is very
of
independent
effectors.
ples
of
independent
effectors.
tractile
responses,
ratherfor
than
serving
ini- than about 1 mm per minute, and all
have
significant
similar
reasons,
have been
been
significant
for
similar
reasons,
ItIt isisstill
stillnot
not clear
clear how
how contractions
contractions spread
spread
tially
for
signal
transmission
over
long
disperhaps
perhaps in
in the
the context
context of
of secretory
secretory or
or concon- attempts
to record
correlates
of
isis very
never
in
Spread
very slow,
slow,
never more
more
in sponges.
sponges.
Spreadelectrical
tances.
Spiking
nerves
transmit
information
tractile
tractile responses,
responses, rather
rather than
than serving
serving iniini- contraction
et
al,
1962;
have
failed
(Prosser
than
than about
about 11 mm
mm per
per minute,
minute, and
and all
all
intially
digital
local depolarizations
for
signal
transmission
over
tially
for form,
signal and
transmission
over long
long disdis- see
also Lawn,
1982).
Somecorrelates
form ofof
attempts
to
electrical
attempts
to record
record
electrical
correlates
of
contribute
nothing
to
the
propagated
sigtances.
tances.Spiking
Spiking nerves
nervestransmit
transmit information
information mechanical
most
likely;
et
1962;
contraction
have
(Prosser
et al,
al,
1962;
contractioninteraction
have failed
failed seems
(Prosser
nal
until
spike
threshold
is
reached;
this
is
in
in digital
digital form,
form, and
and local
local depolarizations
depolarizations for
contraction
one cellform
couldof
see
also
1982).
seeinstance,
also Lawn,
Lawn,
1982).of Some
Some
form
of
crucial
to thenothing
integrative
of the
contribute
to
propagated
sigcontribute
nothing
to the
thefunction
propagated
sig- bemechanical
transmitted
via "almost-desmosomes"
interaction
seems
most
likely;
mechanical
interaction
seems
most
likely;
nervous
system.
Spikes
probably
evolved
nal
nal until
until spike
spike threshold
threshold isis reached;
reached; this
this isis tofor
adjacent
cells,
opening stretch-sensitive
instance,
contraction
of
for
instance,
contraction
of one
one cell
cell could
could
repeatedly,
in
different
plants, of
procrucial
integrative
function
the
crucial to
to the
themany
integrative
function
of
the channels
and
producing
ion fluxes which
be
be transmitted
transmitted via
via "almost-desmosomes"
"almost-desmosomes"
tozoans
and
animals
including
sponges
(as
nervous
nervous system.
system. Spikes
Spikes probably
probably evolved
evolved set
train contractions
in those
cells, and
adjacent
cells,
stretch-sensitive
toin
adjacent
cells, opening
opening
stretch-sensitive
discussed
in in
the
following
section)
onproa soto
repeatedly,
different
plants,
repeatedly,
in many
many
different
plants,
proon,
but
such
a
mechanism
would
channels
which
channels and
and producing
producing ion
ion fluxes
fluxeshardly
which
hoc basis,
using asponges
variety of
more
or less
tozoans
and
including
(as
tozoans
andadanimals
animals
including
sponges
(as represent
"the
germ
from
which
nervous
set
set in
in train
train contractions
contractions in
in those
those cells,
cells, and
and
different
combinations
of
voltage-sensitive
discussed
discussed in
in the
the following
following section)
section) on
on aa transmission
has aagrown."
Unfortunately,
so
mechanism
would
so on,
on, but
but such
such
mechanism
would hardly
hardly
ion
channels.
more
hoc basis,
basis, using
using aa variety
variety of
of nothing
more or
or less
less ad
ad hoc
is known
aboutfrom
membrane
chanrepresent
"the
which
represent
"the germ
germ
from
which nervous
nervous
different
different combinations
combinations of
of voltage-sensitive
voltage-sensitive nels
in
sponges.
transmission
transmission has
has grown."
grown." Unfortunately,
Unfortunately,
ion
channels.
ionSPONGES:
channels.THE "ALMOST" GROUP
Histochemical
tests
indicate
that acetylnothing
isis known
about
membrane
channothing
known
about
membrane
chanSponges are "near-animals" (Parazoa) cholinesterase,
catecholamines and seronels
nels in
in sponges.
sponges.
are present tests
in sponges
with many
"almost"
features.
"On
trouve tonin
SPONGES:
THE
GROUP
SPONGES:
THE "ALMOST"
"ALMOST"
GROUP
Histochemical
indicate
that
acetylHistochemical
tests
indicate(see
thatLentz,
acetyl1968)
but
there
is
no
evidence
des Sponges
'presque
desmosomes',
des
'presque
and
seroSponges are
are "near-animals"
"near-animals" (Parazoa)
(Parazoa) cholinesterase,
cholinesterase, catecholamines
catecholaminesthat
and they
seroinvolved
in signalling
processes
forejonctions
couplage'
et meme
des are
tonin
are
in
(see
tonin
are present
present
in sponges
sponges
(see Lentz,
Lentz,
with
features.
"On
with many
manyde"almost"
"almost"
features.
"On trouve
trouve
Even
plants
'presque
synapses'"
accordingdes
to 'presque
Pa
vans shadowing
1968)
there
no
that
they
1968) but
butnervous
there isisevolution.
no evidence
evidence
that
they
des
desmosomes',
des 'presque
'presque
desmosomes',
des
'presque
have
"neuroactive"
molecules—glycine,
de
Ceccatty
(1989).
They
have
a
mesenare
are involved
involved in
in signalling
signalling processes
processes foreforejonctions
jonctions de
de couplage'
couplage' et
et meme
meme des
des GABA,
glutamate
acetylcholine
(see
chyme
bounded
on allaccording
sides by epithelia,
shadowing
nervous
evolution.
Even
shadowing
nervousand
evolution.
Even plants
plants
'presque
synapses'"
to
'presque
synapses'"
according
to Pa
Pavans
vans Hille,
1984).
but
the
epithelial
cells
are
not
joined
have "neuroactive"
"neuroactive" molecules—glycine,
molecules—glycine,
de
de Ceccatty
Ceccatty (1989).
(1989). They
They have
have aa mesenmesen- have
together
by occluding
so the
Recent glutamate
work on glass
(HexacGABA,
glutamate
and sponges
acetylcholine
(see
GABA,
and
acetylcholine
(see
chyme bounded
bounded
on all
alljunctions,
sides by
by epithelia,
epithelia,
chyme
on
sides
a
much
more
internal
environment
may
not
be
very
well
tinellida)
shows
that
they
have
Hille, 1984).
1984).
but the
the epithelial
epithelial cells
cells are
are not
not joined
joined Hille,
but
together by
by occluding
occluding junctions,
junctions, so
so the
the
together
Recent work
work on
on glass
glass sponges
sponges (Hexac(HexacRecent
much more
more
internal environment
environment may
may not
not be
be very
very well
well tinellida)
tinellida) shows
shows that
that they
they have
have aa much
internal
912
G. O. MACKIE
animal-like conduction system than other
sponges. When the sponge is stimulated
electrically or by touch the flow of water
across the body wall abruptly ceases. This
is almost certainly due to arrest of flagellar
beating. Arrests spread diffusely in an allor-nothing manner at 2.6 mm per second,
a value which falls within the lower range
of action potential conduction velocities in
non-nervous tissues. Thus the whole sponge
stops pumping within a few seconds (Lawn
et al, 1981; Mackie et ai, 1983). Arrest
signals are conducted through the trabecular tissue, a system of fine strands draped
around the spicules which compose the
skeleton of these sponges. The trabecular
tissue is a syncytium, so conduction of electrical impulses from cell to cell would offer
no problem. To demonstrate beyond question that conduction involves propagated
action potentials will require more work
using intracellular microelectrodes (the
material is very awkward to work with) or
whole cell patch recordings but if the present interpretation proves to be correct, this
will constitute another example of actionpotential propagation in tissues other than
nerves. Signal spread by this means is seen
in plants like Mimosa, Dionaea and Nitella
as well as in certain muscles, epithelia and
glands in a variety of animals (see Mackie,
1970; Anderson, 1980).6
T h e histology and pharmacology of
sponges and their apparent ability to conduct action potentials are all suggestive of
an environment in which nerves might have
evolved, but did not. Sponges show that it
is possible to be a metazoan, responding,
behaving and maintaining a well regulated
body form like other metazoans, but without having a nervous system. Early Eumetazoans were also probably aneural. As
nerves evolved, they gradually assumed
receptive, signalling and to some extent
morphogenetic roles, but not to the point
that all traces of the earlier type of orga-
nization were expunged. For Pavans de
Ceccatty (1974, 1989) sponge research is
akin to archaeology, a process by which the
prehistory of the endocrine, immune and
nervous systems is revealed. The group
deserves closer study.
T H E CNIDARIAN NERVOUS SYSTEM:
ELEMENTARY MY DEAR PARKER?
At its simplest, the layout of the cnidarian nervous system is that of a diffuse, twodimensional network of cells combining
sensory and motor functions, whose processes are not differentiated into axons and
dendrites and which conduct impulses in
any direction. On this basis, Parker and
most later workers, have taken cnidarians
as the starting point for neural evolution.
While this simple type of organization can
be regarded as primitive, it does not follow
that cnidarians are incapable of more
sophisticated neural organization or that
the diffuse net itself is necessarily simple
in functional terms. Cnidarians have been
evolving independently for some 700 million years, and have therefore had plenty
of time to improve their nervous systems
and to develop convergent resemblances
with higher invertebrates.7 What follows
addresses the question of just how simple
cnidarian nervous systems really are.
Hydra
Hydra illustrates the simplest type of
neural ground plan. All the neurons have
sensory processes and synapse with other
neurons or with effectors, but it turns out
that there are several morphologically distinct neuronal subtypes. These are distributed in different ways along the body axis
and between ectoderm and endoderm.
Some are enveloped in glial-like epithelial
sheaths, some are not. All the neurons in
7
While sequence data for 5S rRNA place the cnidarians firmly within the main line of metazoan evolution (Hori and Osawa, 1987), 18S rRNA data suggest that they originated either very low down on the
6
Quite recently, a contractile cell network con- main metazoan tree, or independently, within a sepducting electrical impulses at 16 mm-sec"1 has been arate branch including fungi, plants and ciliates (Field
found in the tunic of a didemnid ascidian. There are et ai, 1988). If the latter, it would be necessary to
no nerves or muscles in the tunic and this conducting postulate a quite extraordinary degree of evolutionsystem of interconnected "myocytes" appears to have ary convergence between cnidarians and other metaevolved de novo in relation to regulation of water flow zoa (Bode and Steele, 1989). Reanalysis by Lake (1990)
favors the former.
through the colony (Mackie and Singla, 1987).
ELEMENTARY NERVOUS SYSTEM
the animal are constantly changing their
location. They are lost at the extremities,
and new ones are added in the body column by transformation of interstitial cells.
Not only do established nerve cells change
their locations, but they can undergo morphological and immunochemical transformations as they go (see Bode et al., 1988).
Antisera to six neuropeptides are stated to
recognize distinctive neuronal subsets (see
Grimmelikhuijzen, 1984). Not all the neurons run in diffuse nets: some are concentrated in well-defined bunches or bundles
thought to function as behavioral control
centres. In addition to their behavioral
roles, nerves in hydra may play an important part in the regulation of growth and
in the production of chemical morphogenetic gradients (see Grimmelikhuijzen and
Schaller, 1979; Lesh-Laurie, 1988). Taken
together, these findings suggest that hydra
does not have a very simple nervous system
after all.
Cellular-level neurophysiology in medusae
913
a single, dominant brain in medusae is no
more a sign of primitiveness than it is in
lamellibranch molluscs. A ring-shaped central nervous system is appropriate for a
radially symmetrical animal (Spencer and
Arkett, 1984).
Neurophysiological analyses have been
carried furthest in two hydromedusae,
Polyorchis and Aglantha and in the scyphomedusa Cyanea. It has become increasingly
clear that hydromedusan neuro-muscular
systems have properties similar to those of
other invertebrates. The neurons exhibit
conventional action potentials with sodium
carrying most of the inward current and
potassium the outward, excitatory postsynaptic potentials, miniature end plate
potentials, calcium-dependent, quantal
transmitter release, along with spatial and
temporal summation and facilitation at
their synapses (see Anderson and Spencer,
1989; Spencer, 1990). Patch-clamp analysis has revealed the presence of a family of
A-type potassium channels in Aglantha
reminiscent of the multiple versions of the
A-type potassium channel found in Drosophila (see Meech, 1990). Synaptic delays
as low as 0.7 ms have been recorded at
neuromuscular junctions in the escape
pathway of Aglantha. This species along
with a number of other hydromedusae and
siphonophores has evolved giant axons
capable of conduction velocities as high as
4 metres per second (reviewed by Mackie,
1984). One of the marginal sub-systems in
Polyorchis (the " O " system) consists of electrically coupled, non-spiking oscillatory
neurons which hyperpolarize in response
to a reduction in light intensity, disinhibiting the swimming motor neurons they synapse with (Arkett and Spencer, 1986).
These are just a few of the highlights from
recent research illustrating the fundamental conventionality of hydromedusan neurophysiology. In no way can nerve cells in
these animals be regarded as primitive, if
"primitive" implies that they have gone
only a small distance toward evolving a repertoire of functions comparable to those
found in higher animals.
Most of what we now know about circuitry and cellular-level neurophysiology
in cnidarians comes from studies on hydromedusae and scyphomedusae. These animals lend themselves much better to neurophysiological analysis than do the sea
anemones favoured by Parker, Pantin and
their followers (see Passano, 1982; Spencer
and Schwab, 1982; Satterlie and Spencer,
1987).
In hydromedusae, the nervous system is
concentrated in bundles (nerve rings)
around the margin. These are integrative
centres where peripheral pathways converge, where input from ocelli, statocysts
and other receptors is received, and where
activity patterns are generated. In fact, they
fulfill the same functions as brains in higher
animals and sometimes expand into ganglionic swellings at key convergence points.
In scyphomedusae, as in hydromedusae,
subsets of morphologically distinct neurons interface at ganglionic centres which
also serve as input points for information
coming from the major sense organs and
function as pacemakers producing the
In a nerve plexus designed to spread
swimming rhythm. Complex sense organs, excitation in any direction it would seem
like the eyes of cubomedusae (Piatigorsky desirable to have junctions that can transet al., 1989), may be present. The lack of mit in either direction, rather than having
914
G. O. MACKIE
separate pathways polarized in different
directions within the plexus. Bidirectional
transmission is achieved in hydromedusae
largely by the use of gap junctions, but
bidirectional chemical synapses are also
found in this group and in the scyphomedusae; such synapses appear to be the rule
rather than the exception. Clusters of vesicles are seen on either side of the apposed
membranes. Anderson (1985) has shown
by transynaptic recording that these junctions do in fact transmit in both directions
in Cyanea. He suggests that bidirectional
synapses may arise in development simply
because growing neurons are programmed
to form a synapse whenever they contact
another neuron and that they are not significant as a device for facilitating multidirectional impulse traffic. It seems more
likely to the present writer that this is precisely why they are significant. Whatever
the answer, these junctions are of exceptional interest because each ending is
simultaneously pre- and post-synaptic, and
transmembrane currents can be studied
under voltage clamp. The latest intriguing
finding to emerge from this work (see
Anderson and Spencer, 1989) is the marked
discrepancy between the number of transmitter quanta needed to produce the postsynaptic currents observed and the number of synaptic vesicles present. If one
quantum equals one vesicle, at least an
order of magnitude more vesicles would
be required than are actually present. Nonvesicular quantal release has been described
in other systems (see Dunant, 1986) but is
generally held to be exceptional.
Chemical transmitters
Despite much research and numerous
claims both for and against roles for most
of the classical neurotransmitters and many
neuropeptides in cnidarians, it is still not
possible to say precisely what is going on
at any cnidarian synapse. Anderson (1990)
points out that synaptic delays as low as 1
msec (Cyanea) and 0.7 msec (Aglantha) must
reflect the action of "fast" classical transmitters binding directly to ligand-gated
post-synaptic channels but despite some
claims on behalf of acetylcholine, it has not
yet been possible to show satisfactorily that
any of them function in this way. There is
abundant evidence for the presence of biogenic amines (dopamine, noradrenaline,
adrenaline and serotonin) in cnidarian tissues and for their roles in modulating
behavior, but they have not yet been shown
to function at the level of the individual
synapse (see Anctil, 1990; van Marie, 1990).
Recent work from A. N. Spencer's lab
offers hope for a positive identification of
dopamine as an inhibitory neurotransmitter in Polyorchis. Dopamine is present in
nerves in the nerve rings and recordings
from voltage clamped neurons in culture
show long-lasting outward currents following the application of 10~*M dopamine
(preliminary results cited by Spencer,
1990).
Many (but by no means all) cnidarian
neurons have been shown to contain neuropeptides with either an Arg-Phe-NH2 or
Arg-Trp-NH 2 carboxyterminus (RF- and
RW-amides respectively, see Grimmelikhuijzen et al, 1990). Immunogold labelling shows RF-amide in dense-cored vesicles in hydra (Koizumi et al., 1989) and in
Aglantha (the author, with C. L. Singla,
unpublished), but there have as yet been
no reports of such vesicles concentrated at
synapses. These peptides occur only in
neurons. RF-amides have well-marked
behavioral effects on sea pansies (Anctil,
1987) while in sea anemones, two RWamides have been found to have opposite
effects on antagonistic muscle groups, stimulating one group and inhibiting the other
(see McFarlane et al., 1990). The only studies to be done at the cellular level were on
Polyorchis, where application of RF-amides
produced long lasting depolarizations of
the swimming motor neurons, but this
effect may be an indirect one (see Spencer,
1990).
Thus, while the transmitter picture is still
quite incomplete, it now seems highly
probable that both aminergic and peptidergic transmitter systems occur in cnidarians, supporting Prosser's (1990) argument for the early, parallel evolution of
these two classes of neurotransmitter.
Transmitter release may be localized at
"true" synapses (as in Cyanea) but immunofluorescence microscopy typically shows
RF-amides concentrated in varicosities distributed along the whole length of the neu-
ELEMENTARY NERVOUS SYSTEM
rites, suggesting diffuse release of the peptide and a modulatory or even paracrine
("local hormone") action. For Anctil
(1990), cnidarians may stand at a transition
point between the presumably primitive
paracrine mode of neurohumoral action
and the more advanced neurotransmitter
mode.
Gap junctions and early neural evolution
Hydrozoans are liberally endowed with
gap junctions, which function much as they
do in higher animals, passing dyes and electric currents. An antibody raised against a
27 kD rat liver gap junction protein recognizes a gap junction antigen in hydra and
when introduced into epithelial cells interrupts communication between them,
blocking the diffusion of a morphogen
(head inhibitor) (Fraser et al., 1987).
Impulse propagation via gap junctions
enables many hydromedusan epithelia to
act as sensory or motor adjuncts of the nervous system. Even where no propagated
impulses are involved, gap junctions may
still serve to spread synaptic currents
locally, as in the swimming myoepithelium
of Aglantha (Kerfoot et al., 1985). In the
medusa Polyorchis, several neuronal subsets
running in the marginal nerve rings consist
of coupled groups of neurons, functionally
the equivalent of single large axons (Spencer and Arkett, 1984). Only where such
systems interface with one another or with
effectors are chemical synapses found.
In scyphomedusae and anthozoans a very
different picture prevails. Gap junctions are
not seen by electron microscopy. There is
no evidence to suggest that electric currents, let alone propagated action potentials, can spread from cell to cell within
epithelia. In the only synapses studied, no
coupling or dye transfer was found between
neurons.
It is true that these animals may have the
genes for connexin and are simply not
expressing them, or are expressing them
in a form which has not yet been recognized: "time (and molecular genetics) will
tell" (Greenberg, 1990). On the basis of
present, published evidence however there
appears to be a fundamental dichotomy in
cnidarian evolution separating the hydrozoans from the other two classes (Mackie
915
et al., 1984). This puzzling situation raises
several tricky questions, one of which concerns the proposal that electrical signalling
via gap junctions preceded neural evolution (see above, p. 908). If this is true, the
ancestors of anthozoans and scyphomedusae must have had gap junctions at one
time and lost them during their evolution.
It seems more likely that gapjunctions arose
de novo in the ancestors of the Hydrozoa
after nerves had already evolved, which
argues against the proposal in question.
PROBLEM-SOLVING BY CNIDARIANS
Many of the best examples of complex
behavior in cnidarians are provided by work
on sea anemones (reviewed by Pantin, 1952;
Ross, 1974; Shelton, 1982). Sea anemones
like Calliactis climb up on molluscan shells
inhabited by hermit crabs, responding to
contact with the periostracum. Others like
Stomphia detach from their substrates and
swim by lashing their bodies from side to
side when they sense the presence of a starfish. In one case (Elliott et al, 1989) the
triggering substance has been identified as
imbricatine, a metabolite of the starfish
attacker. In Anthopleura aggressive
responses are shown against non-clone
mates, serving to preserve substrate for the
clone (Francis, 1973). The aggression
response involves leaning over and stinging the victim with nematocysts concentrated on special inflatable structures
(acrorhagi). While some progress has been
made in analysing these and other complex
activities in terms of conduction pathways
and chemical triggers (see McFarlane,
1982; Shelton, 1982), the underlying neuromuscular mechanisms remain obscure.
This is because present techniques do not
allow cellular-level studies to be carried out
on these animals. Workers intent on pursuing the reductionist analysis of behavior
down to the level of individual nerve cells
and junctions have increasingly chosen
hydrozoans and scyphozoans. These studies have yielded important insights into how
behavioral problems are solved in cnidaria,
as illustrated in the following examples.
Problem 1.—In jellyfish like Aglantha and
Polyorchis swimming by jet propulsion
requires synchronous, symmetrical contraction of all parts of the muscle field.
916
G. O. MACKIE
Otherwise, the bell could not contract as
a unit, and swimming efficiency would be
reduced. Ifjellyfish were bilateral, cephalic
animals with front and back ends, they
could employ the sort of device used by
squid and electric fish to synchronize excitation at the two ends of their mantle muscles and electric organs respectively, namely
using faster nerves to excite more distant
effector units. In a radial animal however
the problem is that excitation can originate
anywhere around the 360° perimeter, and
to wire the animal with separate sets of fast
and slow neurons capable of relaying input
in the desired way from all possible points
around the margin would require an enormous number of neurons.
Solutions.—1. Aglantha, whose rapid
escape response involves special circuitry,
uses a single enormous giant axon conducting at up to 2.6 msec" 1 and capable of
spreading excitation all the way around the
ring in as little as 2-4 milliseconds (see
Mackie, 1984). This is the "brute force"
solution.
2. Polyorchis has a more sophisticated
solution. Regardless of where they are initiated, the action potentials conducted in
the ring of motor neurons change shape
as they progress around the margin in such
a way as to excite the muscles with progressively shorter and shorter latencies.
The reduced contraction delay at more distant points compensates for the extra time
taken by the impulses to reach those points.
Spencer and his co-workers must be credited with a imjor tour-de-force in explaining how this all works in terms of events
at the membrane level (Spencer et al.,
1989).8
8
Spike duration is greatest close to the initiation
point because voltage sensitive K+ channels are inactivated when the neuron is depolarized, which delays
repolarization. Accordingly, as the spike progresses
into more hyperpolarized regions, it loses its plateau
and becomes quite brief. Inward Ca++ current in the
presynaptic membrane is maximal in the 0-20 mV
range. During repolarization of a broad spike (which
peaks well beyond this range) calcium entry and hence
transmitter release is considerably delayed, while with
a smaller, shorter duration spike, calcium entry is not
delayed, but is maximal for most of the overshoot,
and transmitter release occurs with a much shorter
latency. Hence EPSPs and muscle contractions occur
with progressively decreasing delay as the distance
from the site of stimulation increases.
Problem 2.—The jellyfish Aglantha has
two swimming requirements: one is for
slow, rhythmic swimming while feeding,
and the other is for rapid escape swimming
when threatened. If Aglantha were a crab,
it would have at least two sets of muscles,
one for fast and one for slow swimming,
matched with separate fast and slow motor
innervations (see Atwood, 1977). Microscopic examination shows however that
Aglantha has only one type of muscle and
only one set of nerves. How are two types
of contractions possible?
Solution.—The innervation consists of a
set of eight giant motor axons running up
into the muscle field. When fired in the
escape mode, these axons conduct sodium
spikes at ca. 4 m-sec"1 which cause fast-rising 98 mV post-synaptic potentials in the
muscles. In slow swimming, the same giant
axons are fired by rhythm-generating axons
in the inner nerve ring and produce not
sodium spikes, but propagated calcium
spikes, conducted at 0.25 msec" 1 , which
cause slow-rising, 56 mV post-synaptic
potentials in the muscles. Thus, the ability
to swim in two ways is ultimately due to
the ability of the motor neurons to conduct
two different sorts of action potential with
differing effects on the muscles (Mackie and
Meech, 1985).
Many more examples of problem solving
by cnidarians could be given: how the sea
anemone Actinia uses one conduction system to mediate two distinct responses,
feeding and escape, using frequency differences in the impulse patterns generated
by chemo- and mechanoreceptors respectively (McFarlane and Lawn, 1990); how
physonectid siphonophores achieve bidirectional locomotion using alternate nervous and non-nervous excitation pathways
to the muscles (see Mackie et al., 1987);
how calycophoran siphonophores broaden
their muscle action potentials progressively in a swimming burst, increasing tension and jet pressure gradually, so avoiding
damage to their trailing appendages (Bone,
1981); how Obelia hydroids spread luminescent responses without nerves using
excitable epithelia and chemical signalling
through gap junctions (Dunlap et al.,
1986)—the list could be a long one. The
lesson emerging from these examples is that
917
ELEMENTARY NERVOUS SYSTEM
cnidarians often make ingenious use of
simple devices to achieve results which
higher animals achieve in more complicated ways. These "typically cnidarian
solutions" (L. M. Passano's phrase) are
marked by parsimony in use of materials.
Simplicity does not mean crudity. The
solutions are elegant. Elegant simplicity is
the hallmark of cnidarian behavior.
EMERGENCE OF HIGHER BEHAVIOR
When it comes to tracing nervous origins
it is hard to dispute Bullock and Horridge's
(1965) conclusion that cnidarians "give
evidence of being too far along in evolution to aid directly in this question." Structurally, the cnidarian nervous system may
seem "elementary" or "primitive" in its
two-dimensional layout and in the limited
diversification of neuron types but in terms
of basic neurophysiological mechanisms, as
we have seen, there is nothing to suggest
that cnidarian neurons differ significantly
from those of higher animals except possibly in the poorly understood area of synaptic transmission. Supposedly archaic features such as unpolarized conduction and
the lack of a single, major ganglionic center can be seen as "ingenious solutions to
problems associated with radial coordination" (Satterlie and Spencer, 1987). Regarding ganglionic functions, (McFarlane
etal. (1990) see "few significant differences
between sea anemones and other invertebrates."
As to advanced behavior, most modern
workers would have to agree with Parker
(1919) in dismissing as inadequate both von
Uexkull's description of sea anemones as
"a bundle of reflexes" and, at the other
extreme, Gosse's picture of them as creatures endowed with consciousness and will.
Cnidarian behavior is characterized by
labile response patterns, and by complex,
internally generated rhythms in addition
to the simpler reflex activities. Unfortunately, there is still little detailed information on the more complex forms of cnidarian behavior as most workers have
concentrated on more readily analysable
aspects. It is not at all clear to what extent
cnidarians can modify their behavior. Classical conditioning has been demonstrated
in some lower invertebrates, e.g., turbel-
larians (see Koopowitz, 1990) but attempts
to do so in sea anemones have been inconclusive (Ross, 1965). Some capacity for
habituation has been shown (see McFarlane
et al., 1990) but there have been few investigations and the mechanisms are unknown.
Toward the end of his career, Pantin
(1965) wrote "it is embarrassing for me to
recall that in my earlier work with Calliactis, the whole animal was treated essentially
as if it were a neuromuscular preparation."
Perhaps now that we have penetrated more
deeply into the circuitry underlying some
cnidarian activities, the time is ripe for a
new look at what Parker was willing to call,
"in its very broadest sense," their psychology.
ACKNOWLEDGMENTS
I am grateful to L. M. Passano, D. H.
Paul, C. L. Prosser, R. A. Satterlie, N. M.
Sherwood and A. N. Spencer for criticizing
drafts of this paper, and to authors of articles in Anderson (1990) who let me see
copies of their papers before publication.
The line "elementary my dear Parker" was
Gabriella Kass-Simon's idea. I thank the
American Society of Zoologists for funding my trip to Boston to deliver this paper
at its centennial meetings in December
1989.
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