Spermatogenesis in Serpulorbis (Mollusca: Vermetoidea) and its implications for phylogeny of gastropods

Abstract

Summary Spermatogenesis in Serpulorbis squamigerus and S. variabilis was studied with light and electron microscopy. In spite of their unusual method of accomplishing internal fertilization by the use of spermatophores, the genesis and structure of vermetid eusperm is in most respects typical of Hypsogastropoda (sensu Ponder and Lindberg, 1997). However, vermetid eusperm have evolved a complex acrosome with a number of unique features not previously described in this taxon. Parasperm of vermetids are easily distinguished by their unique shape, but are more similar in their development to parasperm of some Hypsogastropoda than they are to those of Cerithioidea and Campaniloidea. One feature that was thought previously to provide a link with Cerithioidea and related groups, is the presence of the tail brush in mature parasperm. However, in Serpulorbis variabilis the tailbrush is reduced or lost in some parasperm at maturity and in S. squamigerus it is completely replaced by the terminal bulb, which is synapomorphic with Hypsogastropoda. Also, unlike Cerithioidea, paraspermiogenesis in Vermetoidea always involves the complete elimination of the nucleus and no acrosome is formed. For the first time, nuclear degradation in parasperm of Vermetoidea is shown to progress by an apoptotic mechanism. The many nuclear vesicles that pinch off during this process are broken down by lysosomes secreted by the Golgi body, such that nuclear material is not detected in the mature parasperm. This mechanism of “nuclear apoptosis” is different from that observed in Cerithioidea and Littorinoidea, but is similar to that in some Hypsogastropoda. The Golgi body is involved in producing numerous large glycoprotein granules that fill the body of the parasperm and form a sheath around the axonemal core. This core of axonemes extends anteriorly into a long compound flagellum that produces little motility. Eusperm and parasperm are sealed together inside a spermatophore that dissolves and releases its contents once inside the female reproductive tract. At this point eusperm and parasperm are separate, but in Vermetus alii there is evidence that, prior to this, they form spermatozeugmata in the vas deferens, which is a derived feature characteristic of some Hypsogastropoda. This and other evidence supports the conclusion of Healy (1988b) that Vermetoidea are not closely related to “lower” caenogastropods, such as Cerithioidea. Rather, they are closer in sperm charactersitics to “lower” Hypsogastropoda, which include superfamilies such as Littorinoidea, Stromboidea, Janthinoidea and Triphoroidea.