The malaoologioalmalacological societysooiety of Japan 貝 雑 VENUS （Jap． Jour． Malac ．） −． Vo1 ，48， No ．2 （1989 ） ： 99 139 総 説 Review 陸 生 貝 類 に お け る 生 殖 の ホ ル モ ソ 支 配 武 旧 直 邦 ． 〔東邦 大学 理 学 部 生 物学 教室 ） Hormonal Co1ユtrol of Reproduction in Land Snails Naokuni TAKEDA 〔Department of Biology ， Faculty Qf Science ， Toho University ， Funabashi ， Chiba 274， Japan） CONTENTS I． Introduction ．．．．．．．．，．，，．．▼，，．．．、。，， ．100 1L Neuroendocrine Systems ．．．．．，．．．，．．． ．101 A ． Neurosecretory Systems ．．，，，，．．．，， ，101 B ． Endocrine Organs 、．．．．．．．．．．．．．．．． ．102 a ▼ Dorsal bodies ．．．．▼，．．．，．．．．．．．．．， ．103 b『 Optic glands ．．．．、．．．，，，．．，．，．．．．． 。104 c ． Hermaphrodite glands ．．，．．．．．．．．． ．106 11L Hormonal Control of Reproduction ．．．．，．．．．，．．．．．．．．．．，．，．．．．．．．106 A ． General Morphology of the Reproductive System ．．．．，．．．，．．．．．．106 B ， Maturation of the Reproductive System ．．．，．．．．，．，，．．．，，．．，．．107 a ． Ga 皿 etogenesis ．．．．．，マ．．．．．．，，，．，．．『，呷。．．．．．．，，，，．．，．．．．．『．107 b ． Accessory sex organs ．，，．．．．，，，．．．，．．、．，．．，．，，．．，。．．，，，．，，111 1， Head −warts ．．．．，．．辱，．『．，凸．，レ，．．，，．．，呷，．，．．．の．．．，．『疊．．，．112 2． Albumen glands ．．，，．．，，，．．．．，．，，．，．，．，．．．，．．．．．．．，．．．．113 3． Reproductive tracts ．．．．．．．，，．．．．，．．，．，．． ．，．，．．，．．．，．．．．113 C ． Mating Behavior ．．．．．．．．．．．，．．．．＿ ．，．．，，，．．．，．，．．．．，．．．，，．115 D ． Oviposition ．．．呷．．．．．，．，．呷．．．．．『．，．．．，．．，，．，，．，．．．．．．．．．．．．．118 1V ， Dynamics of 且 ormonal Control of Reproduetion ．．．，．．．．，．．，．．．，，119 V ． Comparative Endoerinology of Reproduction in Molluscs ．．．．．．．．．，121 References ，．，．．．．，．．凾．．．呷．幽．，．．．．．．，．鹽鹽．．．．，．．，．層．．．，．．．．，．．，．．．，，128 一 NII-ElectronicN 工 工 Eleotronio Library Service The malacologicalsocietymalacological society of Japan 100 VENUS: VoL48, No. 2 (1989) Neuroseeretory cells oeeur in the eentral I. Introduction nervous system in all molluscan speeies. Mollusean species show a great diver- In the less organized groups such as sity. They are adapted to a variety of Bivalvia or Prosobranchia, epithelial different environmental conditiens. The endocrine glands are entirely lacking, greatest ranges ef environmental con- as feund in the lower invertebrates ex- ditions that must be survived by organ- cept the Arthropoda. Therefore, neuro- isms are those found on land. Terrestrial seeretions are the only chemical eo- forms are found only in prosobranch ordinators in these speeies. With the 'ehese, and pulmonate gastropods, Among inerease in body eornplexity, endoerine pulmonates are far more suceessful on glands, such as the dorsal bodies and land than prosobranchs. In particular, the optie glands, are developed in highly stylommatophoran species are exelusively erganized speeies such as pulmonate terrestrial and are considered to have gastrepods and cephalopods. Thus, the adapted to the land habitat directly neuroseeretory system and the endoerine from the sea, as they have no fresh- glands so eoordinate reproduction that water aneestors (Joosse, 1979). Slugs mollusean speeies ean propagate them- are eonsidered to have evolved from selves functionally. snails in whiah the shell has degenerated Our knowledge of the hormonal eon- as they have a eommon developmental trol of reproduction en molluses has stage in whieh a cap-shaped shell is inereased (e.g. Boer and Joosse, 1975; formed. Takeda, 1981: Joesse and Geraerts, 1983; With the adaptation to life on land, a Geraerts et al,, 1988; Joosse, 1988). number of physiological ehanges have However, the studies are mainly re- occurred. These are lung respiration, strieted to those on Lymnaea <fresh- highly developed senee organs, a eon- water basommatophoran pulmonates> eentrated nervous system and complex (e.g. Geraerts and Joosse, 1975; Joosse, reproduction, As to reproduetion, all l975; Joosse et al. 1985). ApZysia (ma- pulmonates are hermaphrodites, and the rine opisthobraneh gastropods> (e.g. male and female gametes differentiate Strumwasser, 1984; Arch and Gainer, within a single gonad, called the herma- 1985; Geraerts et al., 1988), and Oetopzts phrodite gland This is different from (cephalopods) (e.g. Wells and Wells, other hermaphrodite animals where 1977; Wells, 1978) and there are cem- there are two different gonads or one paratively few in studies on stylommato- sex succeeds another (Reinboth, 1975). pheran pulmonates (e.g. Gomot et al., All stylommatophoran speeies are true 1980; Takeda, 1982a; Takeda, 1985a; simultaneous hermaphrodites, although Takeda et al., 1986; Gomot and Delay, they may show functional protandry 1987), Therefore, in the present Teview, (Tompa, 1984). In addition, self-fertili- the hormonal control of reproduction of zation and parthenogenesis are also land snails and slugs is diseussed from found in some speeies (Ikeda, 1937; the view point of eomparative endocri- Emura, 1981). nology. The rnain rnaterials are the The reproductive process is generally snails, Euhadra peliotnphala･ and Acha- known to be under the hormonal control, tina fulica, and the slugs, Limax margi- NII-Electronic Library Service The malacologicalsocietymalacological society of Japan Takeda: Hormonal Control of Reproduction in Land Snails 101 natus and DeToce7'as reticulatnm which Ktihlmann, 1964; Gabe, 1966; KUhlmann, are commonly available in Japan. 1966; van Mol, 1967; Boer and Joosse, 1975; Kai-Kai and Kerkut, 1979; van II. Neuroendocrine System Minnen and Sokolove, 1981; Roubos, The endocrine systems serve as bases 1984; Ridgway, 1987). These neuro- foT the control of reproduction, Gen- seretory eells are often unipelar and erally, neurosecretory cells in mollusean show a great variability in size. The speeies are grouped within ganglia and nuclei are lobed and contain large num- are assoeiated with the regions of the ber of nucleoli. Sometimes, they con- perineurium of nerve adjacent to blood tain many inclusions sueh as glycogen, vessels, forming neurohemal areas. His- lipid droplets, lipofuscin and carotenoids, tolegieal changes in these cells are cor- They are located at the periphery of related with a variety of reproduetive each ganglion. A large group of neuro- phenomena. Among invertebrates, the secretory cells is situated in the central species of molluscs and arthropods are and dorsal parts of the mesocerebrum the most highly organized in body struc- apposed to the perineurium elosed to tures and have some endoerine glands. the origin of the eerebral commissure. Many neurohormones released from The axons of these cells form a bundle neurosecretory cells aet direetly on spe- whieh passes into the eerebral neuropile, cifie target tissues, whereas others con- where it branches into a larger and a trol activities of endoerine glands in smaller one. The entire peripheral re- secreting hormones, Thus, in eombina- gion of the nervous systern is used for tion with the neuroseeretory system, the hormone release in most molluscan spe- endocrine glands form an endocrine eies, this is termed peripheral neuro- system whieh in arrangement and scope secretlon. resemble those of vertebrates. Surpris- In Ezthadra peliompha･la and Acha･tina ingly, molluscan hermaphrodite glands fulica, the brain is eovered with the are known to secrete sex steroid thick and hard connective tissue dif- hormones whieh play a similar role in ferent frorn that ot Limax marg･inatus. principle to those of vertebrates. Neuroseeretory eells in the eerebral ganglia were found in the medial, lateral A. Neurosecretory Systems and posterior parts forming a mass. In The central nervous system in mol- these species, medial neurosecretory cells lusean species consists of a number of ehange aetivity in relation to reproduc- ganglia eonnected by commissures and tion: during the breeding season, they conneetives. These are the paired eere- beeome aetive in the produetion and bral (brain), pleural, parietal, pedal release of seeretory materials whereas ganglia and a single visceral ganglion, outside the breeding season their ac- Sinee the first dernonstration of neuro- tivity beeome low. Fine strueture of secretory eells in the Mollusca by the aetive medial neurosecretory eells in SchaTrer (1935) in Pleurobranehea (ma- Euhadrq petiomphala is shown in Fig. rine opisthobranch gastropods), neuro- 1. Many well developed Golgi apparatus, seeretory cells have been deteeted in all which indicate the produetion of seere- groups of molluscs (e,g. Nolte and tory granules, are seen. Neuroseeretory NII-Electronic Library Service The malacologicalsocietymalacological society of Japan 102 VENUS: Vol.48, No. 2 (1989) Fig. 1. Fine structure of the medial neurosecretory of the brain in the snail, -v -? E"hadra PeliomPhala in the breeding season,cells tkMWIo y t.p ( ac ss et6 ma op ･pa me 5> mu pm te oMmaMk,E, materials aTe known to be released fTom has been demonstrated in the nerve cells the cell body or the axonal endings into (Schot et al,, 1981; Joosse and Geraerts, the hemolymph via the neurohemal areas. 1983; Kobayashi et al., 1984; van Noor- In Euhadra peliompha･la and Limax den, 1984; Marchand and Gomot, 1986). marginatt{s, the majority of the neuro- In the present speeies, many neuro- secretory axons run to the neurohemal peptides have been detected in the area, the peripheral regions of the central nervous system (Takayanagi ganglia and others innervate directly the and Takeda, 1984; Takeda et al,, 1985; target organs sueh as the optic gland Fukutomi et al., 1986; Takeda et al., and the dorsal bodies as described later. 1986; Takeda, 1987a; Takayanagi and In the snail, Helix ponati.a, neuroseere- Takeda, 1987; Mizuno and Takeda, tory materials are released into the 1988a,b; Takayanagi and Takeda, walls of the cerebral