On Sperm Storage Organs
How does such short-term mate guarding increase the male’s chances of successful paternity? Species with a single blind-ended sperm storage organ usually show a pattern of last-male precedence in siring offspring, because rival males have the opportunity to actively disrupt or remove any sperm already stored there (e.g., Waage, 1979, 1984) or to passively displace the sperm deeper, rendering it ineffectual (e.g., Lefevre and Jonsson, 1962; Parker, 1970b). However, last-male precedence is not prevalent in species with two sperm storage organs, like littorinid snails, where there is an opportunity for the first male’s sperm to be transferred to the second storage organ before physical interference is possible by a subsequent male.
Besides the number of storage organs present, the shape of the sperm storage organs also has an effect on sperm precedence. Species which exhibit last-male precedence often have a relatively long, tubular, blind-ended storage organ, which is thought to promote stratification of sperm, with older sperm being overlaid by sperm from successive matings (e.g., Walker, 1980; Briskie and Montgomerie, 1993). However, Zeh and Zeh (1994) suggest that though tubular morphology may favor sperm stratification, this relationship breaks down if the storage organ becomes completely filled, which causes increased pressure and induces sperm mixing.
Spherical storage organs are thought to promote sperm mixing (Walker, 1980). In L. obtusata, the bursa copulatrix is the primary sperm storage organ. The bursa is a blind-ended sac, providing the potential for sperm stored there to be disturbed by the penial filaments of rival males. Although there is no evidence of physical sperm displacement from the bursa copulatrix in Littorina, this remains a possibility because penial filaments are extensible and very mobile (Buckland-Nicks, 1974; Buckland-Nicks et al., 1999). The secondary sperm storage organ, the seminal receptacle, is much smaller than the bursa and is situated deep within the pallial oviduct, beyond the reach of the penial filament (Buckland-Nicks and Chia, 1990). The longer a male guards a female, preventing her from participating in further mating, the greater the likelihood of his sperm leaving the bursa copulatrix and becoming stored in the seminal receptacle, to which male genitalia have no access.
Whether female littorinids can selectively store and use sperm from the seminal receptacle is not known. Our results for two of the three broods (A and C) indicate that the males that mated prior to capture had more success than the last males to mate, even though these later males were isolated with the female for up to 3 weeks. Moreover, males from places other than the home locale of the females (Port Bickerton) had little to no success. It is thus possible that females have some ability to stratify sperm in the seminal receptacle or to dump sperm from the bursa copulatrix. In this context, Haase and Baur (1995) suggested that females may be able to manipulate fertilization of eggs by storing sperm in different areas of the seminal receptacle. In L. obtusata, one might expect that the first sperm to reach the seminal receptacle would be stored close to its exit, favoring first-male precedence. However, our results support neither first nor last-sperm precedence and suggest there is mixing of sperm within the female’s reproductive tract.
The results of paternity from the three egg masses of L. obtusata raise some intriguing questions about sperm selection. To fully understand the occurrence of sperm competition or cryptic female choice in these snails, experiments must be designed that track the sperm of individual males inside the female, as well as in the resulting offspring. This might be accomplished by using sperm-specific fluorophores, genetic markers, or the tried and tested method of radioautography (Beeman, 1970).
Ian G. Paterson, Vanessa Partridge, and John Buckland-Nicks