Development of a penis from the vestigial penis in the female apple snail, Pomacea canaliculata.

In the apple snail (Pomacea canaliculata), females have an undifferentiated mass of tissue near the anus. Although this mass is called the vestigial penis, there are no signs of a hermaphroditic gonad or any structure that represents a transition from one sex to the other. Based on considerations of the steroid hormone theory of reproduction and in view of disruption of endocrine systems in molluscs by organotins, a study was made of the effects of tributyltin on female snails. Exposure to tributyltin resulted in the socalled imposex phenomenon, and both a penis and a penis sheath were newly generated from the so-called vestigial penis. The same phenomenon was also induced by testosterone. Thus the vestigial penis, named more than one hundred years ago, has been demonstrated for the first time to be a rudiment of the penis itself. The Ampullariidae (Gastropoda, Prosobranchia, Architaenioglossa) is a family of freshwater prosobranchs that are widely distributed in Asia, Africa, and South America (1). It is well known that some molluscs exhibit unusual sexual diversity and hermaphroditism (2, 3). One of the most interesting features of members of the Ampullariidae is that females in 5 of the 10 genera—namely, Pila (4, 5, 6, 7, 8, 9, 10, 11, 12), Pomacea (13, 14, 15, 16), Lanistes (13, 17, 18), Afropomus (19), and Turbinicola (13)—have a socalled vestigial penis in addition to the normal reproductive system (Fig. 1). The vestigial penis was first described by Bouvier (4, 5), a skilled neuroanatomist, in Ampullaria (Pila) polita more than 100 years ago. Since then, many molluscan researchers have used that term for this tissue without further explanation. The question examined here is this: Is the organ historically described as a vestigial penis a remnant of a penis—a degenerate structure that lacks the capacity to develop further—or is it a rudiment, or precursor—an incipient structure that, under the proper conditions, could develop into a penis? The vestigial penis is a tongue-like structure lying inside the elevated mantle skirt, near the anus (Fig. 2A). Histologically, it consists of connective tissue, and no differentiation of the structure is apparent during the life cycle of the female (Fig. 2B). To my knowledge, no experimental evidence has been presented to justify the designation of the elevated tissue near the anus in some female snails as a “vestigial penis” (4, 5). No clear evidence of hermaphroditism has yet been shown in any extant species of Ampullariidae. In Pomacea canaliculata, the apple snail, the positions of the gonads are basically different: the testis is located at the tip of the spiral, and the ovary is spread over the surface of the hepatopancreas at a location similar to that of the testis. It has also been confirmed that there is no apparent precursor or vestige of a hermaphroditic condition in any part of the reproductive system throughout the life history. As Andrews (13) stated, the copulatory apparatus appears to develop at the same rate in both sexes until the gonad becomes active, when its growth is arrested in the female. Andrews hypothesized that the gonad might produce a hormone responsible for the cessation of growth, but in the early 1960s, when this work was published, the chemical nature of reproductive hormones in molluscs had not yet been established. In 1991, Berthold (20) proposed that the so-called vestigial organ be designated an “oriment”—a term implying that the tissue is a precursor with the potential to develop into an adult organ. The question then arose as to whether such a designation might be appropriate. As a basis for such a designation, at the very least, some experiments involving implantation of testes into females should be performed to determine whether a true penis might develop from the tissue mass. Received 7 December 1999; accepted 10 August 2000. E-mail: [email protected] Reference: Biol. Bull. 199: 316–320. (December 2000)