Spawning as an endocrine-controlled event

Spawning in marine invertebrates has been reviewed recently (see Giese & Kanatani, 1987 see also Schroeder, 1984), and it is at once clear that in only very few species is the endocrine control mechanism understood in any detail.

The endocrine control of spawning in starfish is well documented (see Shirai etal, 1986; Meijer & Guerrier, 1984). It involves a gonad stimulating substance (GSS), released from the radial nerve, acting on the gonad, to produce a maturation inducing substance (MIS). Gonad stimulating substance is a thermostable 22* amino acid neuropeptide of about 2100 Da which is released from neurosecretory granules in the radial nerve (Kanatani et al, 1971). Maturation inducing substance on the other hand was identified as a purine, 1-methyladenine (1-MeAde) (Kanatani etal, 1969) and is released from the interstitial glands of the testes and the follicle cells of the ovary following stimulation by GSS. The action of 1-methyladenine on the oocyte is to reinitiate meiosis, and because oocyte maturation can also be induced by certain fatty acids it is thought that these, or other related acids, may play a role in transducing the signal from 1-methyladenine across the cell membrane (Meijer etal,

1984; Meijer ef al, 1986a). It has been demonstrated that exogenous arachidonic acid is converted to hydroxy-metabolites by the oocytes and of these that only (8R)- Hydroxyeicosatetraenoic acid (8-HETE) and not (8S)-HETE are capable of stimulating oocyte maturation (Meijer et al, 1986b).

As an endocrine substance, 1-MeAde has a multiplicity of roles in the induction of spawning (see Meijer & Guerrier, 1984 for review). It stimulates not only the maturation of the oocytes, but also their separation from the follicle cells

and the contraction of the ovarian wall (Shirai et al, 1986). The separation of the follicle cells is thought to be attributable to endogenous protease activity, whilst ovarian contraction occurs, probably, by the action of a contraction inducing factor. The action of 1-MeAde on the oocyte is to stimulate the production of an active factor in the oocyte cytoplasm (see Kishimoto, 1986), and it is this ‘Maturation Promoting Factor* (MPF) that is responsible for oocyte maturation. As spawning commences, 1-MeAde stimulates reproductive posture in both sexes, and because this can be induced in spent animals, it is assumed that in this aspect 1-MeAde acts on the nervous system directly (Shirai etal, 1986).

Spawning in the mollusc Aplysia has also been the subject of detailed investigation (see Giese & Kanatani, 1987) and the mechanism which underlies the release of eggs in the female is reasonably well understood. Egg laying is induced by the action of egg laying hormone (ELH) which is a neurosecretion released from the bag cell cluster of cells associated with the abdominal ganglion (Kupfermann, 1972) and has been identified as a single polypeptide of 36 amino acid residues (Chiu et al,, 1979). The hormone is released from stimulated bag cells and the electrical coupling of individual cells is such that the release of ELH is synchronised and is sufficient to stimulate egg laying (Kupfermann & Kandel, 1970). The target cells for ELH are thought to be small muscle cells which surround each follicle in the ovotestis (Coggleshall, 1970; 1972). As well as acting to release oocytes, ELH also modifies the behaviour of the animal and induces such behaviour as puckering of oral musculature, weaving head movements and infrequent locomotion (Arch & Smock, 1977).

In the molluscs Haliotis nifescens and Mytilus califomianus, spawning is thought to be stimulated by the action of a prostaglandin endoperoxide enzyme (Morse et al, 1977; Fitt & Trench, 1981). This observation is however, derived

from the the use of specific inhibitors and stimulators of prostaglandin endoperoxide synthetase and therefore no detail is available on the specific mechanisms involved.

The endocrine control of spawning in other invertebrates has been demonstrated in relatively few species. In the coelenterates, spawning in the medusa Spirocodon saltatnx occnxs in response to a spawning inducing substance which is produced during darkness (Ikegami et al,, 1978). The substance is thought to have a low molecular weight and is produced in the ovaries.

In three species of polychaetes endocrine mechanisms have been identified. In Nephtys hombergi, spawning is brought about by the release of a spawning hormone from the supraoesophageal ganglion (Olive, 1976; Olive & Bentley, 1980; Bentley, 1986a). This causes rhythmic contraction of the body wall musculature and results in the ejection of gametes from the coelom to the exterior via the pre- pygidial rectal cleft and the anus (Bentley, et al, 1984). Experiments have also suggested that the normal behaviour of spawning animals is modified by spawning hormone and gives way to violent spasmodic contractions of the body during spawning (Bentley, 1984). Preliminary purification of spawning hormone, suggest that it is a trypsin sensitive, heat stable peptide of between 2,000 - 4,000 daltons (Bentley unpublished observations).

In Pectinaria gouldii a factor from the suboesophageal ganglia and the cement gland brings about maturation and spawning of gametes in both sexes (Tweedell, 1980). The biological activity of this factor is destroyed by heating, and dialysis suggests that it is a molecule of larger than 12,000 daltons. Tweedell noted that it brought about the maturation of the gametes which includes the release of spermatozoa from sperm packets and germinal vesicle breakdown in oocytes, and he suggested that the entry of oocytes into the nephromixia was possible only once maturation had taken place.

The maturation and spawning events observed in Pectinaria are very similar to those of Arenicola marina. These will be discussed in greater detail in section 1.5, although it is important to say here that gamete maturation in Arenicola occnts in response to a maturation factor released from the prostomium. During maturation, oocytes of Arenicola marina^ undergo passage from the first prophase stage of meiosis to the first metaphase stage and this is accompanied by germinal vesicle breakdown (GVBD) (Howie 1961b; Meijer 1979a). In males, sperm dissociate from sperm morulae to become free swimming (Howie 1961a; Meijer 1979b). Spawning follows this gamete maturation in that eggs and sperm which have not undergone this final maturation are rejected by the nephromixia which act as gonoducts and are therefore retained within the body cavity. Gametes which have undergone their final maturation however, are accepted automatically and shed (Howie 1961b & c; Howie 1962).

Franke & Pfannenstiel (1984) pointed out that despite the similarity of their function (in that they both bring about spawning in sexually mature animals) the maturation hormones of Arenicola and Pectinaria both differ considerably from the spawning hormone of Nephtys in their mode of action. Only in Nephtys does the hormone act as a true spawning hormone by stimulating muscular activities which lead to gamete release whereas, in both Arenicola awA Pectinariay spawning relies upon maturation of the gametes brought about by the respective endocrine factor.

There are several common characteristics of endocrine substances throughout the examples outlined in this section. The stimulation of muscular contractions which result in gamete release is an important although not exclusive feature of such substances. Often they display a multiplicity of roles in several target tissues and may exert their effects indirectly. In many situations they also act to modify the animals behaviour in some way; the reproductive posture of starfish (see Meijer & Gurrier, 1984), the head waving behaviour of Aplysia{see Arch &

Smock, 1977) and the muscular contractions of Nephtys{see Bentley, 1984), are all either direct or indirect effects of the spawning hormone.