Download "I`ll see it when I believe it!"*: Investigating Nervous System

AMER. ZOOL., 29:1141-1155 (1989)
"I'll see it when I believe it!"*: Investigating
Nervous System/Reproductive System Interactions
in Animal Organisms1
LOUISE RUSSERT-KRAEMER
Department of Zoology, University of Arkansas,
Fayetteville, Arkansas 72701
SYNOPSIS. From the time of August Weismann's characterization of fundamental differences between the role of the reproductive system (to preserve the "immortal" germplasm)
and the other, somatic tissues of the organism (to maintain the organism) biologists have
inherited an interesting organismic conundrum. How, indeed, are we to understand the
relationship between the somatic systems (especially the nervous system—that characterize
the animal organism) and the reproductive system, within that organism? In this paper it is
argued that: (1) neuron-gamete-organism interactions are essential, organismic phenomena that have scarcely begun to be investigated; (2) with reference to at least three different
kinds of animals it is possible to determine developmental, structural, functional and
behavioral relationships between the (species-oriented) reproductive systems, and the (individual, organism-oriented) nervous systems of those animals; and (3) results of such investigations make sense only in terms of the peculiar evolutionary history and environmental
adaptations of specific kinds of animal organisms.
tive behaviors as isolating mechanisms
influencing
evolution. In the ethologically
August Weismann presented zoologists
enthusiastic
1960s, however, a number of
with a conundrum that is still engaging:
the continuity ("immortality") of the zoologists seemed to persuade themselves
germplasm and contrasting discontinuity that animal behavior was either immedi(mortality) of the somatoplasm of the indi- ately or ultimately all reproductive behavvidual animal organism. While zoologists ior (Marler and Hamilton, 1967). It could
today could scarcely be found to subscribe be argued that an extreme extrapolation
to a fundamentalist view of his argument, from the latter is to be found in a current
Weismann's early and important effort to view, promulgated by Dawkins (1982) and
distinguish between the very different others, that the organism is essentially a
functions of reproduction (to maintain the gene-container for future generations of
species) and "vegetative activities" (to its species.
Mintz (1975) may, inadvertently, have
maintain the organism), certainly influenced the direction of subsequent studies provided a basis for a new perspective on
of zoologists. In the early decades of this relationship between reproductive cells and
century, for example, zoologists pursued somatic cells. She found that malignant
studies that revealed the definable seques- tumor cells could be experimentally introtering of the germplasm in eggs, zygotes, duced into the normal tissues of certain
embryos and differentiated animal organ- mouse embryos, and there would give rise
isms. In later decades, other investigations to germ cells and somatic cells (including
revealed that much of an animal's behavior nerve cells). These and other findings prorepertoire is composed of reproductive duced by various lines of research make it
behavior (the biological basis for which lies evident that there is as yet no clear underessentially in the animal's nervous system). standing of just what distinctions can be
Early comparative ethologists sensed the made between germ cells and somatic cells
importance of species-specific reproduc- such as nerve cells. Furthermore, many
zoologists doubt that: (1) animal organisms
can be regarded as hierarchic extensions
1
From the Symposium on Is the Organism Necessary? of the great Gene-Machine; or that (2) a
presented at the annual meeting of the American vertebrate-physiology model of hypothaSociety of Zoologists, 27-30 December 1987, at New
lamic-gonadal pathways can be adequate to
Orleans, Louisiana.
INTRODUCTION
1141
1142
LOUISE RUSSERT-KRAEMER
investigate and interpret reproductive system/"somatic systems" interactions. Still,
the existence, nature and biological implications of reproductive-nervous system
relationships within the organism have as
yet hardly been thought about for most kinds
of animals.
Through the years, no matter what forces
have moved the winds of fashion in scientific research in zoology, zoologists have
shared the perception that the reproductive system of an animal, more than any
other system, functions to maintain that
animal's species. Zoologists have also
repeatedly realized that the nervous system, more than any other system (not
infrequently including neurendocrine tissues)—functions to develop and maintain
the individual animal. A research preoccupation that must develop in the coming
decades, one may argue, will take on the
question, "What are the developmental,
structural, functional, and behavioral relationships between the (population, speciesoriented) reproductive system of specific
kinds of animals, and the (individual, organism-oriented) nervous system of those animals?"
In this paper some nervous system/
reproductive system interactions will be
reviewed. It will be shown that these interactions make sense only in terms of the
peculiar evolutionary history, anatomy,
physiology and behavior of the particular
animals under scrutiny. Such interactions
have been found and examined in bivalved
mollusks, especially in the freshwater
unionid mussel species, Lampsilis ventricosa
(Barnes), and in the introduced Asian clam,
Corbiculafluminea(Muller). Just how these
animals involve their nervous tissues in distinctive, developmental and seasonal
responses to their reproductive cells and
systems will be presented and analyzed
here. Two other examples will be employed
as well, one a vertebrate, the parthenogenetic lizard, Cnemidophorus uniparens, and
the other a cnidarian, Hydra sp. From the
foregoing the argument will be developed
that there really are organisms in the world
that have to be studied as organisms; for
they are not understandable as simply ganglionic preparations, or, for that matter,
as mere vector points in a population analysis.
RESULTS OF GERMANE STUDIES ON
THREE KINDS OF ANIMAL ORGANISMS
The "case" of Cnemidophorus uniparens
(Reptilia: Lacertilia)
The all-female, parthenogenetic species
of lizards, Cnemidophorus uniparens, and C.
laredoensis (Order, Sauria; Family, Teiidae)
have been the focus of intensive investigation in recent years (e.g., Cuellar, 1979;
Cole and Townsend, 1983; Walker, 1986,
1987; Paulissen and Walker, 1989). In these
species, it seems apparent that the lizard's
neurendocrine system and its reproductive
system are functionally interrelated,
though in an unlikely and puzzling manner. The realization that there must be such
an interrelationship stems from the
repeated observations that have been made
of male-like, pseudocopulatory behavior (its
biological basis lodged in the neurendocrine system) of the parthenogenetic lizards, in captivity. Why and how does reproductive behavior, characteristic of dioecious
(gonochoristic) lizard species, persist in
parthenogenetic species? Crews and his colleagues (Crews et ai, 1986) found that the
pseudocopulatory, male-like behavior of
certain parthenogenetic (female) lizards
actually facilitated reproduction in other
parthenogenetic (female) lizards. They
reasoned that the evolutionary background of the parthenogenetic lizards
could provide a clue (Crews et ai, 1986, p.
5949),
This persistence of pseudosexual behaviors and behavioral facilitation of reproduction is perhaps due to the fact that
the species arose from the hybrid union
of 2 gonochoristic species (species with
males and females).
Why would individual lizards of a parthenogenetic species exhibit mating behavior? Cole and Townsend (1983) reported
that no difference in reproductive output
could be found from parthenogenetic lizards reared in isolation, and those observed
to participate in pseudocopulation. Nonetheless, Crews et al. (1986) reasoned that
NEURON-GAMETE-ORGANISM INTERACTIONS
since behavioral facilitation of reproduction is known to occur in gonochoristic
species of Cnemidophorus, something of the
sort might also be occurring in C. univalens.
With intensive monitoring of the gonadal
condition and the behavior of caged lizards, it was found that (Crews et al., 1986,
p. 5949),
Female-like, pseudosexual behavior is
limited to the pre-ovulatory stage of the
follicular cycle, whereas the expression
of male-like pseudosexual behavior
occurs most frequently during the postovulatory stages of the cycle. . . . This
alternation in behavioral roles is paralleled by transitions in the circulating
concentrations of sex steroid hormones
produced by the ovary.
There are extensive implications in such
findings. Subsequent experiments have
shown that male-like, pseudosexual behavior regularly seen (in lab conditions) in C.
uniparens, in postovulatory lizards, appar-
ently stimulates and facilitates gonadal
development in pre-ovulatory lizards. Workers find that in animal species various
androgens, especially testosterone, are
"essential" to male sexual behavior (Prosser, 1973). Crews reasons that male-like,
pseudosexual behavior in C. uniparens is
triggered, it seems, by a surge in progesterone in the postovulatory, parthenogenetic lizards. From such organism-referenced investigations, Crews concludes
(1987, p. 121),
. . . courtship behavior between (parthenogenetic) females has provided new
insights into behavioral evolution and the
means by which neurendocrine mechanisms that control behavior adapt to
changing conditions.
Some scientists working on Cnemidophorus univalens are concerned that no one has
seen male-like or female-like pseudosexual
behavior in nature, even though the behavior has been seen by a number of workers,
occurring in caged animals (Cole, 1983;
Paulissen and Walker, 1989). Others (Cole,
1983) have noted that many of the captive
behaviors seen in the parthenogenetic
species (diploid C. uniparens and triploid C.
1143
univalens) have also been seen in gonochoristic species, between females. It can
be argued that the very fact that pseudosexual behavior occurs, however, may constitute reason for the controversy, and justifies questioning the present status of the
neurendocrine basis of such sexual behavior in C. univalens.
The "case" of Hydra (Cnidaria: Hydrozoa)
During the 1960s, Allison Burnett and
several of his colleagues at Case-Western
Reserve University in Cleveland, Ohio,
carried out a series of studies on Hydra, in
which they emphasized experimental
attempts to understand the function of
interstitial cells in the body wall of Hydra
(Burnett and N. A. Diehl, 1964a, b; Burnett et al., 1964; F. A. Diehl and Burnett,
1964, 1966). Results of the studies implicated interstitial cells as the stem cells both for
neurons and for gametes. Indeed, Burnett et
al. reported that they could apply special
supravital staining techniques they had
devised to Hydra, in such a way as to destroy
all of the animals' nerve cells (and concomitantly all of their behavior)! Hydra thus
treated, if maintained with care, would
subsequently regain their behavior and
were found, upon examination, to have
regenerated a full complement of nerve
cells, apparently from interstitial cells
(Burnett et al, 1964).
Further, Burnett and his colleagues
found that if nerveless Hydra were maintained in such a way as to inhibit regeneration of the nerve cells, the interstitial
cells in the behaviorless animals developed,
instead, huge masses of gametes (Burnett
et al., 1964)! This work had a special significance that Burnett and his colleagues
were not concerned with at the time. The
work was done at a time of great enthusiasm for research in another area of biology, that of animal behavior. It was a time
when many investigating ethologists and
comparative psychologists were imbued
with the idea (mentioned above and reiterated here for emphasis) that an animal's
behavior repertoire was either proximally
or ultimately concerned with the function
of reproduction. Though it was not a stated
objective of their work on Hydra, results
1144
LOUISE RUSSERT-KRAEMER
tion) recently explained that a population
of interstitial cells has been identified as
the source of neurons in Hydra. The latter
cells have been named "JD-1" cells. More
recently another population of cells has
been found that differentiate into male
gametes (Littlefield and Bode, 1986). The
latter cells have been named "AC" cells.
A search is now underway for a population
of interstitial cells capable of differentiating into female gametes, for which the
hopeful name of "DC" cells is ready.
Workers in the 1980s have thus greatly
refined and amplified relationships between
gametes and nerve cells in Hydra, a relationship that had been experimentally
roughed out in the 1960s, from fundamental organismic studies of Burnett and
his colleagues.
In recent years workers have been able
to kill, selectively, interstitial cells (and not
other cell types) in the body wall of Hydra,
by treating the animals with chemicals such
as colchicine, or with gamma irradiation.
The "nerveless" Hydra can be maintained,
and come to consist eventually, entirely of
FIG. 1. Photograph of gravid specimen of Lampsilis epithelial cells—lacking not only nerve
ventricosa (Barnes) engaged in flapping behavior in the
Fox River, Wisconsin. The mussel is upended, headed cells, but cnidocytes and gametes as well
into the current, and well embedded in the substrate. (Marcum and Campbell, 1978; Wanek et
(Photograph by Marian Harvlik.) AS, anal (incurrent) al., 1980). These "epithelial Hydra" have
siphon; BS, branchial (incurrent) siphon; E, "eye- been used to refine their investigators'
spot"; DO, distal pore in ovisac; LV, left shell valve;
understanding of many vegetative funcO, portion of left, posterior outer gill, serving as martions of the epithelial cells (Marcum and
supium and charged with glochidium larvae; RMF,
Campbell, 1978). Are the "epithelial
right mantle flap; T, "tail" (anterior end) of left mantle flap. Horizontal field width = 7 cm. (From Krae- Hydra" organisms? No. Indeed, such invesmer, 1984)
tigations now seem to have moved from
the quest for understanding of neuronof Burnett and Diehl's experiments showed, making, gamete-making and the interstitial
in contrast, that with destruction of their cells that make both in Hydra. It is noneneurons, the biological basis of the behav- theless important to realize, as Pearse et al.
ior of Hydra—the little animals could only (1987) note, that interstitial cells, when
revert to sexual reproduction! Recent transplanted into the "epithelial Hydra"
development of the work on interstitial cells give rise to gametes with the characteristics
in Hydra has involved several groups of of the donor, not the recipient, Hydra. Even
researchers on the west coast of the U.S. though the "epithelial Hydra" lack interand a group at the University of Tubingen stitial cells, and thus the capacity for makin West Germany. In the 1980s investi- ing either gametes or neurons, the epithegators have concerned themselves with lial preparations can be used in such trials
sophisticated effort to determine the plu- to determine individual attributes of the
ripotency of Hydra interstitial cells (Little- organism.
field, 1984, 1985, 1986; Littlefield and
At present, new work on descendant linBode, 1986).
eage of interstitial cells in Hydra has lately
Beverly Marcum (personal communica- led to development of controversy among
NEURON-GAMETE-ORGANISM INTERACTIONS
1145
researchers on the relation of the interstitial cells to nerve cells and to gametes. It
now begins to appear (once more!) that the
same interstitial cells may give rise to neurons and to gametes (Littlefield, personal
communication).
The "case" of Lampsilis (Mollusca: Bivalvia)
BS
FIG. 2. Series of diagrams showing paired pulsing
movement of mantle flaps in the freshwater mussel,
Lampsilis ventricosa (Barnes), a) position of flaps before
initiation of pulse; b) flaps showing initiation of pulse
at base of the "tails" of the flaps; c, d) flaps showing
progression of pulse movement toward "eyespot" ends
of flaps; d) flaps have reached "eyespot" ends of flaps,
causing them to bend outward. Horizontal field width
Among the large, highly diversified family of freshwater bivalve mussels, the
Unionidae, species of the genus, Lampsilis,
appear to be the most highly evolved. Ortmann (1911) and a few others had observed
that mature mussels in some species of
Lampsilis develop "mantle flaps" that can
exhibit rhythmic movements. It was subsequently found (Kraemer, 1970) that only
mature females possess fully differentiated
"mantle flaps." Kraemer (ibid.) found that
mantle flap movements occur only when
the mature female is gravid. The mussel's
larvae are glochidia, pinhead-sized organisms that must contact gills or fins of a specific fish host, there to embed themselves,
grow, differentiate and live as parasites until
they metamorphose and drop off into the
substrate, where they complete their development into free-living mussels.
The mantle flaps differentiate from each
lobe of the mantle, immediately adjacent
and anterior to the branchial (incurrent)
siphon of the mussel. Though of varying
contour from one mussel species to
another, the flaps have a distinct, fringed
"tail" portion at the anterior end of the
flap, and a striking "eyespot" at the posterior end of the flap (Fig. 1). The flapping
movement is due to a pair of pulses that
originate at the "tail" end and proceed to
the eyespot end of each flap as shown in
Figure 2 (Kraemer, 1970). During flapping
behavior the gravid female mussel typically
upends herself in the substrate, using her
foot as a prop, and often angling herself
into the current of the river. She extends
her mantle flaps and begins to move them
= 5.5 cm. AS, anal siphon; BS, branchial siphon; E,
"eyespot"; O, ovisac of marsupial gill, engorged with
glochidia; T, "tail" end (anterior end) of flap. (Modified from Kraemer, 1970)
1146
LOUISE RUSSERT-KRAEMER
in a sequence of pulsing movements. In ance of the mantle flaps, in dissimilar flapLampsilis ventricosa (Barnes), the mantle flap ping behaviors, and in sensitivity to various
movements reach a rate of three pulses per stimulus modalities (exhibited by the flaps,
second (Kraemer, 1970). To the human siphons, marsupial gills and foot)—quite
observer the paired, pulsing mantle flaps likely relate to differences in the behaviors
distinctly resemble a swimming minnow. of the specific fish hosts of the mussels'
In several species of Lampsilis in which flap- larvae.
ping behavior was studied in detail by
During a flapping behavior period in L.
Kraemer (1970), it was noted that one or ventricosa, an occasion that may last for two
both of the charged marsupial gills would weeks or more (Kraemer, 1970), the gravid
be pushed out from the mantle cavity, to mussel, at dawn, moves into a "headstand"
a position between the pulsing flaps, filling and initiates flapping movements (Fig. 3).
out the "body" of the apparent "minnow." At dusk, the gravid mussel slows her manIn L. ventricosa, a tiny hole was found to tle flap movements, withdraws the flaps and
appear at the distal edge of each marsupial hunches down into the substrate once more
ovisac. Glochidia were seen to disappear (Kraemer, 1970). L. ventricosa has been
from each ovisac during flapping behavior found, experimentally, to increase the pulse
(Kraemer, 1970).
rate of mantle flap movements in response
Each of the species investigated mani- to increments of light at low light intensity,
fests different kinds of flapping behavior mimicking "dawn" (Kraemer, 1970). Sim(Kraemer, 1970). The flapping behavior of ilarly, L. ventricosa has been experimentally
some is diurnal, occurring during daylight, found to decrease mantle flap movements
between dawn and dusk. Others flap just in response to decrements of light at low
as readily in the dark as in the light. The light intensity, mimicking "dusk" (Kraemussels of some species are more sensitive mer, ibid.). The above phenomena are
to jar of the substrate than to light. Some shown in Figure 3.
flap slowly (at a rate ofjust one paired pulse
Careful dissection of the nerves extendper 20 min or more). Flapping behavior, ing from the large, fused visceral ganglion
overall, is reproductive behavior that (located on the ventral surface of the posachieves connection of the parasitic glo- terior adductor muscle) into the mantle
chidia larvae with their respective species reveals extensive, anastomosing innervaoffish host (Kraemer, 1968, 1970; Krae- tion of the regions of the mantle flap in L.
mer and Swanson, 1984). The pulsing flaps ventricosa (Fig. 4). In addition there is, adjamay constitute "lures" (Welsh, 1933) or cent to the "tail" of each mantle flap, what
not, though it seems unlikely (Kraemer, appears to be a large anastomosis (Fig. 4).
1970; Kraemer and Swanson, 1984). When the latter is removed, embedded,
Extensive monitoring of flapping behavior sectioned and stained, however, it is found
in mussels in natural streams, and in mus- to be a distinct, well-organized mantle gansels maintained in the laboratory, showed glion, with a fibrous connective tissue capthat mussel flap movements typically stop sule, a "rind" of neuronal soma and an
when a putative fish host swims near. Not internal neuropil (Kraemer, 1967, 1984).
only that, but the mantle flap movements The mantle ganglia do not appear in the
show obvious habituation (Kraemer, 1969). neuroanatomy of the mantle of juvenile
Recent study has shown that the "eye- mussels. They are not present, either,
spots" are not innervated, and may indeed among the innervating anastomoses of the
perform an effector rather than a sensory mantle of the mature male, even though
function (Kraemer and Swanson, 1984). At the male does develop rudiments of mantle
any rate, the flapping behavior does pro- flaps (Kraemer, 1967, 1984).
vide a vital opportunity for both aerating
In brief summary, in the freshwater musand buoying up the released, non-motile, sel genus, Lampsilis, the nervous system can
glochidia larvae in the water column (Krae- commandeer many of the otherwise trophic
mer, 1970). Species differences in the systems of the foot, gills, mantle and musgenus, Lampsilis, in characteristic appear- cles, to establish the "headstand" stance
1147
NEURON-GAMETE-ORGANISM INTERACTIONS
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FIG. 3. a-d) graphs showing changes in rate of mantle flap movements in gravid specimen of the freshwater
mussel, Lampsilis ventricosa, at times of small increments and decrements of light at low light intensities, a)
flapping rate at dawn; c) experimentally induced increase in flapping rate in response to increments of light
at low light intensity (="dawn"); b) flapping rate at dusk; d) experimentally induced response to decrements
of light at low light intensity (="dusk"). (After Kraemer, 1970)
11
1148
LOUISE RUSSERT-KRAEMER
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FIG. 4. Drawings showing mantle innervation in the freshwater mussel, Lampsilis ventricosa. Top, drawing
showing ventral surface of the visceral ganglion and its main nerve trunks extending posteriorly into the
siphon and mantle, and anteriorly into the gills and visceral mass (horizontal field width = 4 cm); bottom,
drawing showing innervation of region of mantle near the mantle flap of a mature female (horizontal field
width = 3 cm). Note the mantle ganglion (MG) in the female, that is not present in the male. A, anus; AS,
anal siphon; BS, branchial siphon; LMG, left marsupial gill; MG, mantle ganglion; PAM, posterior adductor
muscle; VG, visceral ganglion. (After Kraemer, 1984)
required for the peculiar "mantle-flapping" behavior that attends shedding of
glochidial larvae. During ontogeny of the
female nervous system, developing neural
and sexual dimorphism results in the differentiation of a pair of peripheral mantle
ganglia, each with its own connecting
nerves to the visceral ganglion. Location
of the mantle ganglia, immediately adjacent to the "tail" ends of the females' mantle flaps, where the flapping pulses originate, makes these small peripheral ganglia
NEURON-GAMETE-ORGANISM INTERACTIONS
obvious candidates for "pacemakers" of the
pulsing mantle movements.
Discovery of peripheral mantle ganglia
in Lampsilis is, upon reflection, not surprising. A careful examination of the histology of nerves in these mussels reveals
that the neuronal soma are not confined
to ganglia, but may stream out along commissures and connectives (Kraemer, 1967).
Neuronal soma in such animals thus could
predictably be capable of forming clusters
in peripheral tissues of the bivalved animals. The discovery was surprising for two
other reasons, however. First of all, it was
surprising that the ganglia had not been
found by other workers, years earlier. Perhaps this was because others had not carefully observed the mussels' flapping behavior, and consequently had not thought it
worthwhile to undertake tedious dissections of the mussels' peripheral nervous
system. Secondly, it was surprising to discover that there can be sexual dimorphism
of the nervous system in dioecious bivalves,
that is clearly related to reproductive
behavior of the animals.
A residual suspicion from the foregoing
study is that if nervous systems and reproductive systems in one group of bivalved
mollusks are developmentally, structurally, functionally and behaviorally intertwined, such intimate jugglery is very likely
occurring in other bivalves, and in other
kinds of organisms that manifest structural
and functional plasticity of their nervous
systems (such as vertebrates!) as well.
The "case" o/Corbicula (Mollusca: Bivalvia)
In the United States, between the 1950s
and the 1970s, extensive destruction of the
habitat of indigenous unionid bivalves such
as Lampsilis occurred from California to
Florida, as most large rivers, especially in
the southern two thirds of the states, were
heavily dredged and dammed. In the wake
of that multi-billion dollar, federal enterprise, an introduced Asian clam, a talented
opportunist in the human-damaged habitat, became the most prevalent species of
mollusk, and, in a number of instances, the
most prevalent animal species in the aquatic
ecosystem. U.S. biologists were initially
perplexed as to the identity of the clam.
1149
Was it one species or several? They knew
almost nothing about the biology of the
clams. Yet biologists were aware that the
introduced clams, having established a huge
biomass in the rivers, had become a special
scourge of nuclear-powered utilities, where
the clams cause devastating "clam clogs"
in the cooling water systems—necessitating costly plant shutdowns (Kraemer, 1976,
1978, 1979; Britton, 1979). It was imperative to obtain basic biological information
about the clams. As a consequence of the
First (Britton, 1979) and then the Second
International Corbicula Symposium (Britton, 1986), the clams were provisionally
identified as belonging to a single species,
Corbicula fluminea (family, Corbiculidae)
apparently initially introduced from mainland China, into the Columbia River in the
1930s. Valuable details of the biology of
the clams began to emerge.
Early studies in my laboratory of many
serially sectioned clams provided the finding
(Kraemer and Lott, 1977; Kraemer, 1978)
that the clams are proto-oogamous, making oocytes before they develop sperm,
unlike the protandrous habit (sperm
develop before eggs) of their supposed
indigenous relatives, the pill clams and fingernail clams (Sphaeriidae). That unanticipated finding alone turned out to have
significant consequences for "management" of the clams (Kraemer and Galloway, 1986). Further, several unpredictable
relationships between the reproductive and
nervous systems of the clams were discovered, that (1) form a rational basis for monitoring techniques for the clams; and (2)
contribute to accumulating evidence of a
multiplicity of heretofore unsuspected,
reproductive-neural interrelationships in
bivalves.
It was found that before there is any sign
of gonadal differentiation in C. fluminea,
paired gonopores differentiate on either
side of the postero-dorsal margin of the
visceral mass as shown in Figure 5b (Kraemer, 1978). Location of the gonopores coincides
with the site of bilateral penetration of the
visceral mass by the large cerebrovisceral con-
nectives. The connectives extend all the way
from the visceral ganglion (located ventral
to the massive, posterior adductor muscle),
1150
LOUISE RUSSERT-KRAEMER
cvc
FIG. 5. Photomicrographs of ontogeny of reproductive and innervating processes in the Asian clam, Corbicula
jiuminea (Muller). a) micrograph showing differentiation of oogenic follicle in association with wall of intestine
(horizontal field width = 150 /im); b) micrograph showing differentiation of oogenic follicle in association
with wall of digestive gland (horizontal field width = 300 Jim); c) micrograph showing sprouting of neuronal
fibers from cerebrovisceral connective to innervate lip of gonopore. The neuronal sprouting accompanies
oogenic development shown in "a" and " b " (horizontal field width = 4 mm), d) follicular ganglion that appears
within lumen of spermatogenic follicle at region of confluence with oogenic follicle. Note distinct innervation
by slender nerve (N) from cerebral ganglion (horizontal field width = 0.16 mm). CVC, cerebrovisceral
connective; D, digestive tract; DC, digestive gland; GD, gonoduct; GP, gonopore; N, nerve; NP, neuropil of
follicular ganglion; O, oocyte; SF, spermatocytes, surrounding ganglion, all located in the lumen of a spermatogenic follicle; VMS, stroma of visceral mass, (a, b, c from Kraemer, 1978; d from Kraemer, 1984)
NEURON-GAMETE-ORGANISM INTERACTIONS
1151
forward to the cerebral ganglia (located on regions of confluence between the mature oogenic
either side of the mouth). Subsequently, follicles and the differentiating spermatogenic
oogenic follicles initiate differentiation, follicles, follicular ganglia appear (Fig. 5d)
typically in association with the basal lam- (Kraemer, 1978, 1985). The ganglia are
ina of the epithelium of the intestine of the covered with evident neuronal soma that
clam (Fig. 5a). Oogenic follicle differentia- surround a feltwork of nerve fibers. The
tion also occurs alongside the basal lamina ganglia are connected by small, well-difof the epithelium of the clam's digestive ferentiated nerves to the cerebral or pedal
glands (Fig. 5b). As soon as oogenic follicle ganglia (Fig. 5d).
development is initiated, the cerebrovisceral conWhat is the function of these peripheral,
nectives sprout new nerve fibers that innervate follicular ganglia? The ganglia are surthe lips of the gonopores (Fig. 5c).
rounded by spheres of mature sperm. The
Another, heretofore unsuspected rela- ganglia may have a role in sperm maturationship between the developing repro- tion. The only report in the extant literaductive and nervous systems of C. fluminea ture that appears to refer to anything comdevelops somewhat later in the ontogeny parable to the follicular ganglia of C.
of the clam. As noted above, oogenic fol- fluminea is that of Archie (1941, reported
licles initially differentiate in association in Roosen-Runge, 1977) who characterwith the basal lamina of digestive tube or ized an apparently similar structure (though
digestive glands. Growth of the oogenic he reported no innervation of it) in a snail,
follicles is accompanied by maturation of as a mass of "nurse cells." The location of
the oocytes within the follicles. The mat- the follicular ganglia of C.flumineawithin
urational sequence has been worked out the lumen of spermatogenic follicles that
through analysis of serial sections (Krae- are immediately confluent with the lumen
mer, 1978). The oogenic follicles grow, and of oogenic follicles containing mature
ramify through much of the visceral mass, oocytes indicates a possible role for the
permeating it. At this time, the lumen of ganglia in (self-) fertilization. Indeed, in
each follicle is nearly occluded by the large, serial section study one not infrequently
yolk-laden oocytes. The foregoing findings observes embryos in the vicinity of the ganhave been corroborated with many glia (Fig. 6).
hundreds of dissections of freshly killed
Intensive study of C.fluminea,then, has
clams, carried out for more than two and revealed intimate developmental relationa half years, monthly, weekly, and in some ships between nervous and reproductive
instances, daily (Kraemer and Galloway, systems of the clams: (1) the apparently
1986).
simultaneous "sprouting" of fibers from
It is at this point (to continue reporting cerebrovisceral nerves to innervate gonothe developmental sequence of events) that pores, right at the time oogenic follicles
spermatogenic follicles differentiate from some initiate differentiation; (2) the later differof the peripheral, oogenic follicle walls. Sper- entiation of "follicular ganglia" within
matogenesis now occurs. We have been able spermatogenic follicles as spermatogenesis
to determine, again from voluminous dis- is completed. Certainly the relationship
sections of fresh tissues of clams collected between the foregoing events and the
at close, regular intervals for nearly three reproductive and neural physiology of C.
years (Kraemer and Galloway, 1986)—that fluminea invite further study. In addition
spermatogenesis is not only seasonal in these findings further stretch our limited
occurrence, but is triggered by a specific understanding of the biology of reproducincrease in water temperature (to 19°C for tive systems and nervous systems, and their
10 days) in the spring, and a specific surprising interrelationships, in animal
decrease in water temperature at the end organisms.
of the summer. We realize that spermatogenesis, indeed, "paces" the entire reproCONCLUSIONS AND DISCUSSION
ductive cycle {ibid.). Serial-section study
In this paper results of essentially organrevealed that within the visceral mass, at ismic researches carried out on three very
1152
LOUISE RUSSERT-KRAEMER
FIG. 6. Photomicrographs showing embryological events coinciding with the development of follicular ganglia (shown in Fig. 5d) in the Asian clam, Corbiculafluminea.The micrographs were made from sagittal serial
sections of animals collected in August, in the Buffalo River in northwest Arkansas: a) photomicrograph
showing embryo (E) within spent oogenic follicle. Horizontal field width = 450 mmu. b) photomicrograph
showing embryo (E) within gonoduct of mature clam. Horizontal field width = 4 mm. c) photomicrograph
showing embryo (veliger) with velum (V) in area of confluence between oogenic and spermatogenic follicles—
also the site of the follicular ganglia. Horizontal field width = 200 mmu. The foregoing examples (a-c) have
been cited as evidence of self-fertilization in C. fluminea (see, e.g., Kraemer et al., 1985). E, embryo; GD,
gonoduct; GP, gonopore; LOF, lumen of oogenic follicle; SVM, stroma of visceral mass; V, velum.
different kinds of animals have been sum- Bizarre phenomena categorized in these
marized, and briefly evaluated. In the par- animals suggest a heretofore unsuspected
thenogenetic lizard species of the genus, evolutionary role that may be played by
Cnemidophorus, the role of pseudocopula-sensitive neuronal and/or neurendocrine
tory behavior is being explored as a key to cells in a vertebrate, in the changing
basic relationships between nervous, endo- requirements of the parthenogenetic
crine and reproductive systems in animals. reproductive system.
NEURON-GAMETE-ORGANISM INTERACTIONS
In the cnidarian, Hydra, fundamental
experimental questions are being asked
concerning not only the multipotency of
the animal's interstitial cells, but also the
functions of the interstitial cells in establishing neurons (and concomitantly furnishing the biological basis for the animal's
behavior), and female and male gametes.
Intensive research on "epithelial hydras"
in recent years has made possible the devising of sophisticated hypotheses about the
nature of organismic differentiation and its
genetic basis.
In the bivalved mollusk, the freshwater
mussel, Lampsilis ventricosa, discovery of
peripheral ganglia that are linked to characteristic reproductive behavior of the
gravid female implicates these small,
peripheral mantle ganglia as obvious candidates for "pacemakers" of the pulsing
flaps.
In another bivalved mollusk, the introduced Asian clam, Corbicula jluminea,
as
indicated above, embryological development of the oogenic follicles is associated
with sprouting of nerve fibers from nearby
cerebrovisceral nerves that innervate the
lips of the gonopores. Later, development
of spermatogenic follicles peripherally to
the maturing oogenic follicles is accompanied by the differentiation of follicular
ganglia in areas of confluence between
oogenic and spermatogenic follicles—ganglia that are innervated by small nerves
attached to the cerebral or pedal ganglia.
With both of the mollusk examples, intimate developmental relationships between
differentiating nervous and reproductive
structures appear: (1) to stem from the phylogenetically peculiar, plastic capability of
molluscan neurons to migrate along nerves
to form special-function, peripheral ganglia; (2) to produce much of the behavior
repertoire of the mature bivalve organism;
and (3) to provide the basis for re-production of the populations to which the bivalves
belong.
The cases reviewed above constitute a
body of data that certainly requires rethinking of a certain historical, biological
perspective. The traditional perspective
needing scrutiny, especially by organismal
zoologists, is that while an animal's nervous
1153
system does indeed initiate and maintain
development of structure, function and
behavior of the individual animal, the
reproductive system is primarily organized
to continue the species to which the animal
belongs. How else is one to account for the
fact that the kinds of intimate jugglery,
within the animal organism, between
reproductive and nervous systems—such
as the specific examples reviewed above—
are not yet being regularly sought out by
investigating zoologists? The immediate
agent of nature for establishing the organism certainly appears to lie within the
gametes, and subsequently within the differentiating zygote. Too, while the organism develops, germplasm is at once sequestered from the cascading differentiations
that are occurring in the embryo. However, the moment-to-moment controller of
the possibilities patterned in the gametes
for animal organisms—most often turns
out to be the nerve cell. In developing animal organisms, neurons maintain inhibiting, controlling oversight, not only of
trophic actions but of prospective reproductive activities of the animal, as well.
Nerve cells do not do this alone. Nerve cells
especially have assistance from gametogenic processes occurring within the
organism. Neuronal-gametogenic relationships, such as have been delineated above,
actually help to define the organism.
G. E. Moore argued that the property of
goodness supervenes on physical properties (Moore, 1903). Analogously, it seems
that biological properties supervene on
biochemical reactions in organisms. These
interactions make biological sense when
one thinks of them in an organismal context. One does not have to think of an
organism as a neovitalistic activity. One
does not have to push fluids or spirits. One
can think of the organism as creating sets
of possibilities for occupying space and
engaging in complex activities.
This has been an effort to show that only
an organism-referenced or organismic
approach would make sense of many, many
phenomena that one can observe in different kinds of animals. If an adequate biological understanding of organisms is to be
possible, it should not be dictated solely by