Biological reproduction is an extremely complex process affecting
and involving the animal organism in general and the reproductive
organs in particular. It is accompanied by modifications in the
morphology, physiology, and behavior of animals. Production of
haploid gametes (and their union in a diploid zygote), or diploid
eggs in parthenogenetic organisms, is a crucial moment of
biological reproduction in metazoans. These diploid cells are
uniquely able to develop into a new organism.
The zygotic genome per se, as well as the genome of any
metazoan cell, is incapable of inducing the development of a
multicellular organism. Increasing evidence points to the
irreplaceable role of the epigenetic parental (maternal and
paternal) information provided in the form of cytoplasmic factors
(RNSs, proteins, hormones, neurotransmitters, nutrients, etc.) in
the zygote for the early embryonic development.
Adequate evidence shows that the CNS controls the reproductive
activity and oogenesis, including the crucial process of synthesis
and placement of parental cytoplasmic factors, in metazoans.
Neuroendocrine Regulation of
the Gonadal Function in Insects
Extensive studies on insects show that the insect brain determines
“whether”, ”when”, and “how much” of gonadal hormones will be
synthesized and secreted. The control of the development of gonads
in insects essentially implies processes of cell differentiation
resulting from differential patterns of gene expression in
different cells of the ovary and the reproductive organs in
general. These processes take place under the control of JH
(juvenile hormone), ecdysteroids (E), and neuropeptide
gonadotropins (De Loof et al., 2001) (figure 3.1).
Figure 3.1.
Diagramatic representation of the neural control
of ovarian function in insects.
Abbreviations: PTTH,
prothoracicotropic neurohormone (From Cabej, 2004c1).
Secretion of JH (juvenile hormone) is cerebrally regulated by
various types of neuropeptides that reach CA (corpora allata)
not only via the haemolymph but directly as well, via the NCA I
(nervi corporis allati I) innervating corpora allata.
In other insects, the SOG (suboesophageal ganglion), via NCA II
(nervi corporis allati II) carries out a similar
regulatory function on the JH secretion by CA (Kou and Chen,
2000). In Manduca sexta, dopamine released by nerve endings
in the corpora allata stimulates JH secretion in vitro for
the first two days of the last larval prepupal period (Granger et
al., 1996).
Besides its well-known role in insect metamorphosis, in insects JH
acts as a regulator of the gonadotropic cycle. From this
standpoint, JH itself is a gonadotropic hormone produced by the
endocrine glands, CA. Its secretion is regulated by two types of
neuropeptides secreted by neurosecretory cells in the insect
brain, allatostatins and allatotropins. These neurohormones,
released via the nerve endings in CA cause, respectively,
inhibition and stimulation of JH synthesis (Stay et al., 1996). In
the brain of the cricket Gryllus bimaculatus, 5 members of
the family of allatostatins are identified, and 14 other
neuropeptides have been deduced from cDNA, all of them capable of
inhibiting the JH biosynthesis in vitro (Witek and
Hoffmann, 2001).
The cerebral control of the function of CA, production of JH,
ovarian development, ovulation, and oviposition are accomplished
not just by brain neuropeptides allatotropic and allatostatic
neuropeptides. Experimental evidence on an immediate regulation of
all the above functions by the CNS in insects is also
accumulating: universal neurotransmitters appear to be essential
regulators of these functions. So, e.g. octopamine, a biogenic
amine, inhibits the CA function in the cricket Gryllus
bimaculatus and stimulates oviposition in the common house
cricket, Acheta domesticus (Linnaeus,1758) (Adamo, 1999)
and another neurotransmitter, dopamine, is essential for the
ovarian development and CA activation (Bloch et al., 2000).
In eusocial insects, such as some ants, reproduction is exclusive
function of queens, which produce a pheromone that prevents the
rest of genetically female ants in the colony from reproducing. As
long as these ants remain in the colony their JH level is lower
than is necessary for the maturation of oocytes. This inhibitory
role of the pheromone may be mediated by biogenic amines such as
dopamine; the pheromone is perceived in the insect brain, which
responds to it by lowering the level of the dopamine and by
inhibiting the reproductive activity (Boulay et al., 2001).
Production and secretion of sex pheromones by the sex pheromone
gland in some moths is under control of the neuropeptide PBAN
(pheromone biosynthesis-activating neurohormone) secreted by
secretory neurons Br-SEG (brain-suboesophageal ganglion). The
neurohormone performs its pheromonotropic function by regulating
production of pheromone-synthesis enzymes. The Br-SEG stimulates
secretion of PBAN in response to external cues, such as
photoperiod. Since the neurotransmitter octopamine is demonstrated
to induce pheromone production (Christensen et al., 1992), it is
possible that its direct target cells are PBAN-synthesizing
neurons. Pheromone secretion is inhibited after mating as a result
of the neural signal arising from the sperm storage in spermatheca
(Delisle et al., 2000).
In honey bees, the queen excretes from its mandibular gland a
pheromone, consisting of a blend of chemicals, which prevents the
development of ovaries in workers and inhibits development of new
queens in the colony. It is demonstrated that the pheromone
performs its effects on the behavior (reduced locomotor activity
and nursing) and physiology of worker bees by acting
on central neurons, altering their cellular properties and
changing the output of neural circuits in the brain (Beggs et al.,
2007).
The key component of the pheromone is HVA (homovanillyl alcohol or
4-hydroxy-3-methoxyphenylethanol), which interferes with
the brain dopamine system that is responsible for the development
of the ovary (Beggs et al., 2007).
Mating stimulates sexual maturation in Drosophila females.
It has been shown that a male sex peptide (SP),
produced by the male accessory gland,
and
introduced with seminal fluid during mating,
induces reduction of the female receptivity and increased
oviposition. The peptide induces secretion of JH by corpora allata
(Moshitzky et al., 1996),
alongside other
brainsignals,
allatotropins. Besides, the control of gonadal function via
production of JH by CA (corpora
allata),
cerebral allatostatins may act directly on the oocytes, as it is
suggested by the fact that they (allatostatins A1 and B1) are
found in the cortical cytoplasm of the oocytes (Witek
and Hoffmann, 2001).
Recently, it has been found that the female irreceptivity to
courting males, after the introduction of the male SP with the
seminal fluid, is determined by the insect CNS. From the female
reproductive tract, via the haemolymph, SP circulates throughout
the insect body, including the insect brain (by crossing the
blood-brain barrier). However, only the insect CNS is receptive to
it because it is the brain and the VNC (ventral nerve cord) only
that expresses its specific receptor, SPR. Male derived SP binds
its specific receptor, SPR in the fru-expressing neurons of
the suboesophageal ganglion (SOG) and of the ventral nerve cord (VNC),
which determine the switch to the post-mating behavior of
unresponsiveness to male courting (Yapici et al., 2008).
Two neuroactive substances produced in the brain of the
primitively eusocial wasp (Polistes chinensis), dopamine
and serotonin, are found in its ovary and are involved, the first
in the ovarian development and appearance of egg-laying behavior,
and the second, probably, in regulation of reproductive states of
the insect (Sasaki et al., 2007).
External cues, such as social conditions and/or specifically male
sexual stimuli are necessary for the reproductive development and
ovarian maturation in the dampwood termite Zootermopsis
angusticollis (Brent and Traniello, 2001). These stimuli, via
sensory pathways, reach the CNS where they are processed in neural
circuits, whose chemical output start signal cascades determining
reproductive changes in the genitalia.
Empirical evidence suggests that in the fire ant, Solenopsis
invicta Buren, the queen releases a pheromone that prevents
reproduction of virgin females as long as they remain in the
parental nest (Fletcher and Blum, 1981). The pheromone is thought
to decrease JH production in CA by decreasing the dopamine level
in the brain (Robinson and Vargo, 1997), or via the dopaminergic
innervation of CA (Granger et al., 1996). A brain neuropeptide
hormone, LTE (Lymnatria testis ecdysiotropin), secreted by
the neurosecretory cells of the brain, and by some ganglia in
Lymnatria dispar, is found to stimulate ecdysteroid synthesis
in testis but not in the prothoracic gland. The testis ecdysteroid
then induces the synthesis of a growth hormone that stimulates the
development of the male genital tract (Loeb et al., 2001).
In all the above cases, the environmental cues trigger signal
cascades that induce reproductive activity and oogenesis in
insects. All these cascades start with the release of brain
signals, neurotransmitters or neuropeptides.
Local Neural Control of the
Reproductive Function in Insects
In insects, the CNS is involved in the reproductive behavior and
in the reproductive activity not only via neuroendocrine pathways
but also directly via the local gonadal innervation.
For almost one century, since it was first described, no specific
function was attributed to the nerve innervating the ovotestis in
pulmonate snails, but recent studies on the slug Helix aspersa,
have shown that the OT (ovotestis) branch of the intestinal nerve
consists of as many 3025 axons, suggesting that approximately 8%
of the total number of neurons of the CNS are involved in the
innervation of the slug ovotestis.
From an evolutionary viewpoint, such a costly investment could not
have evolved if it would not offer an outweighing advantage.
Indeed, recently it has been demonstrated that the innervation has
important functions for receiving and sending information from the
ovotestis to the brain and, vice versa, from the brain to the
ovotestis. The innervation is necessary for maturation of oocytes
and ovulation. It has both sensory and motor functions. The fine
terminals of the OT nerve branch have stretch sensors in the
acinar walls, which monitor the degree of stretching as a result
of the concurrent growth of over 100 oogonia. That information on
the stretch, via afferents, is sent to the brain, where it is
assessed and, when it exceeds a threshold, efferent brain signals
are sent back for increasing peristaltic contractions in the
hermaphroditic duct and the beat of the cilia in the internal
lining of the duct, thus facilitating the movement down the duct
and oviposition of 58 to 108 egg cells (Antkowiak and Chase, 2003;
Chase et al., 2004).
Neuroendocrine Regulation of
Reproductive Function in Vertebrates
In vertebrates as well, reproductive functions are cerebrally
controlled, mainly via the hypothalamic
à pituitary
à gonadal axis. In
cyclical ovulators, the reproductive activity is stimulated by
environmental factors such as temperature and moisture, but above
all by the seasonal changes of the day length (in most cases its
prolongation): the onset of reproductive activity starts with
displays of mating behavior, which is determined by activation of
specific neural circuits, in response to visual and auditory
stimuli. In birds, e.g., as a result of the activation of the
hypothalamus-pituitary-gonadal axis, gonads are stimulated to
synthesize testosterone, and high levels of this hormone play a
crucial role for the onset of mating behavior in males. This leads
to increased conversion of testosterone into estrogens in the
birds’ brains, thus contributing to the full display of the male
mating behavior, in which several neural circuits are involved.
