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Hermaphroditism in molluscs

Biological journal of the Linnean Society 1993 v.48 no.1 pp. 19-42
Bivalvia, Gastropoda, aquatic invertebrates, brooders, embryogenesis, endocrinology, genitalia, habitats, hermaphroditism, hosts, males, molluscs, osmotic stress, parasites, parthenogenesis, population density, predators, selfing, sex determination
The functional significance of hermaphroditism is, as yet, not well understood. This study attempts to examine the relevance of some theories on this topic to reality, by reviewing the literature on hermaphroditism among molluscs. The study reveals that about 40% of the 5600 mollusc genera are either simultaneous or sequential hermaphrodites. Hermaphroditism occurs in 100% of the Solenogastres, 99% of the Opisthobranchia, 100% of the Pulmonata, 3% of the Prosobranchia and 9% of the Bivalvia. Sequential hermaphroditism, whatever its theoretical advantages over gonochorism, is not common among molluscs. Simultaneous hermaphroditism is common among the Euthyneura. Over 80% of the hermaphroditic genera belong to the Euthyneura (about 2000 recent genera), and over 99% of the Euthyneura are hermaphrodites. The almost ubiquitous occurrence of hermaphroditism throughout the Euthyneurans, coupled with this group's very widespread dispersal in marine, terrestrial and freshwater habitats (and corresponding exposure to a very wide range of predators, competitors or parasites); and also its wide range of population densities, suggests that in this group hermaphroditism is not an adaptive response to selective forces of the environment and it may well be a phylogenetic constraint. A few stylommatophorans have broken this constraint by possessing genitalia in which the male system is absent (aphally) or extremely reduced (hemiphally). They reproduce by self-fertilization. In theory this is advantageous in that these species save the cost of developing two sets of reproductive apparatus. In reality there is no record of aphally occurring throughout an entire species, as one may expect if this saving of cost were so overwhelmingly advantageous. There is also no record of stylommatophoran individuals developing only the male system, as one may expect if there was any evolutionary trend from hermaphroditism towards gonochorism. Simultaneous hermaphroditism offers a (theoretical) option to selling. Selfing by self-fertilization is widespread among freshwater basommatophorans, amphibious stylommatophorans and freshwater bivalves. Selfing by parthenogenesis is widespread among freshwater prosobranchs. Altogether, of 48 genera which self, 60% are dwellers of freshwater. Certain freshwater habitats may perhaps be less stable than most marine or terrestrial ones are. Beyond the Euthyneura, hermaphroditism is common among parasitic, deep sea and Cnidaria-eating molluscs. Perhaps these three associations should be slightly rearranged and combined into a single generalization: that hermaphroditism (beyond the Euthyneura) is widespread among molluscs that live in a close and permanent intimacy with live marine invertebrates, whether as parasites, commensals or predators. Gonochorism but with dwarf males is common among the Eulimoidea, which are parasites, and Galeommatoidea, which are commensals. This situation of gonochorism, in which there is a very close association between members of the two sexes, is functionally a hermaphroditic type. Animals that can manipulate the physiology and endocrinology of their hosts may also have the tendency and ability to manipulate the size of their own males. It may well be that the female not only determines the size of the male but also his sex, in which case dwarf males should be considered as a case of environmental sex determination. The theoretical possibility that hermaphroditism may evolve in brooding animals was examined in gastropods. Among the (predominantly gonochoric) prosobranchs brooding is recorded in 85 genera (4%), only two of which are hermaphrodites. Among the (predominantly hermaphrodite) heterobranchs it is recorded in only 95 odd genera (4%). When all gastropod genera are considered together, the frequency of hermaphroditism among the brooders is only very slightly and insignificantly higher than in the non-brooders. When only the prosobranchs are considered, the frequency of hermaphroditism among the brooders is actually lower than among non-brooders. The theory that hermaphroditism evolves in brooding animals thus appears not to be relevant to the vast majority of gastropods. Brooding is widespread among freshwater prosobranchs (48% of the brooding genera). In this habitat, brooding may perhaps be an adaptation to protect the developing embryo against osmotic stresses.