Freshwater Pulmonate (Mollusca: Gastropoda) Reproduction
by Rachel Sommer
BIOL/WATER 361, Fall 2013
Living in freshwater comes with its share of difficulties. One of the challenges to overcome is being able to reproduce and bring young into the world that will also be able to reproduce. For all organisms, being able to reproduce viable offspring equals a successful life. Freshwater pulmonates, snails, have overcome the challenges of reproducing in ever-changing freshwater habitats by being hermaphrodites. Hermaphroditism is a common sexual reproductive strategy found throughout freshwater invertebrates. In the case of freshwater pulmonates, being hermaphroditic arose from a number of morphological and physiological changes made as pulmonates evolved to live on land and eventually, for some, in freshwater. Because of their hermaphroditic anatomy, freshwater pulmonates are capable of cross fertilizing, as well as self-fertilizing. The reasons and ramifications of out-crossing and selfing are important for the continued survival of pulmonates species in freshwater environments. By exploring the anatomy, physiology, and copulation methods of hermaphroditic snails, cross fertilization and self-fertilization can be further understood, all in an effort to unravel how and why freshwater pulmonates reproduce as they do.
Being hermaphroditic means an individual freshwater pulmonate is able to produce both eggs and sperm, as part of a diploid adult lifecycle. Spermatogenesis and oogenesis occur within the same gonad, the ovotestis. Depending on the species, male and female gametes may be formed in the same or different sacs, acini, within the ovotestis (Collier, 1997). Egg and sperm leave the ovotestis via a common hermaphroditic duct. The gametes are separated into male ducts and female ducts. The male duct ends with the penis, which is located behind the head. The female duct is made up of multiple glands, which assist in egg packaging. Just before the female genital pore, which is located by the aperture of the shell, there is a seminal receptacle, where sperm from another individual is stored. The ability to produce male and female gametes at the same time in their life makes freshwater pulmonates simultaneous hermaphrodites.
Even though freshwater pulmonates may be generalized as simultaneous hermaphrodites, there is strong evidence that sperm production begins before eggs reproduction. In the case of many species including Biomphalaria glabrata, Lymnaea stagnalis, and Physa fontinalis, laboratory studies report the production of sperm precedes the production of eggs by several days to a few weeks (Dillon, 2000; Trigwell & Dussart, 1998). Having a distinct period of male reproductive function prior to a female function is referred to as protandric sequential hermaphroditism. However, the time freshwater pulmonates solely function as males is considered to be too short to be significant, and is more aptly referred to as being “slightly protandric” simultaneous hermaphrodites (Trigwell & Dussart, 1998). Attaining male sexual maturity first may occur for a number of reasons. As younger males, freshwater pulmonates may be able to practice copulating and subsequently produce more offspring in the long run. Smaller male actors, it seems have an easier time fertilizing another individual, as the female actor may display less rejective behaviors (Dillon, 2000).
Copulations between freshwater pulmonates include one individual acting as a male and another individual acting as the female. Mating is initiated by the male acting individual. The acting male finds, follows, and eventually mounts the shell of the individual that will act as the female. Mounted females are known to display a range of rejection behaviors including: shell shaking, wrinkling, withdrawing, lifting, and in some species, biting. All of these behaviors are made in an effort to make the genital pore inaccessible. Freshwater pulmonates that have recently been inseminated and those that have not mated as male or female have a tendency to display these behaviors at a greater magnitude (Dillon, 2000). If the male manages to stay mounted and everts his penis, probing causes the female actor to stop rejection behavior and submit to the copulation. Copulations take anywhere from a few minutes to over an hour to complete.
After the male actor successfully transfers sperm to the female actor, a reciprocal copulation may occur, in which the roles are reversed, or the freshwater pulmonates go their own way. Other copulation methods that have been recorded include; simultaneous reciprocal copulation and chain copulations. Simultaneous reciprocal copulation involves two individuals transferring sperm to each other at the same time. This is accomplished in certain species through a very specific body alignment. Chain copulations involve multiple individuals acting as a male and a female at the same time (Trigwell et al., 1997).
After a successful insemination, the received sperm in the female tract is either degraded or kept for fertilization. The seminal receptacle holds and stores received sperm. Sperm may be stored for more than 3 months, in Lymnaea stagnalis (Loose & Koene, 2008). Due to this sperm storage and the possibility of multiple copulations, post copulatory competition exists. Therefore, it is expected for freshwater pulmonates have a way of determining a potential partner’s mating history. A recent study found that L. stagnalis, after isolation, will donate more sperm to an unmated partner than to a partner previously mated (Loose & Koene, 2008). Another post-copulatory competition method is a copulatory plug. After insemination, the male actor will leave a temporary plug in the female actor’s genital pore, in an attempt to stop a competitor’s sperm from fertilizing the female actor’s eggs (Dillon, 2000).
So far, reproduction in freshwater pulmonates has been discussed in the context of two or more individuals involved in the process of fertilization. This is referred to as, out-crossing, the use of received sperm to fertilize eggs. It is the most common method of fertilization. However there is a significant amount of self-fertilization known to exist among freshwater pulmonates. In studied species, such as Physa acuta and Bulinus forskalii, fertilization solely from out-crossing rarely occurs (Henry et al., 2005; Gow et al., 2005). Instead a mix between out-crossing and self-fertilization in each egg mass seems to be most common. Research conducted on self-fertilizing freshwater pulmonates aims to understand, under what circumstances and to what extent self-fertilizing is occurring, especially since self-fertilizing is closely associated with an inbreeding depression.
Self-fertilization in freshwater pulmonates may occur for a number of reasons. One idea is that somewhere along the shared male and female ducts of these simultaneous hermaphrodites, there is an imperfection. This imperfection allows male gametes and female gametes to meet, and self-fertilization accidentally occurs (Dillon, 2000). Another thought is that self-fertilization, instead of being an evolutionary mistake, is possible as a reproductive assurance. Freshwater snails are found in a wide variety of habitats, from ephemeral streams to large perennial bodies of water. Within these habitats an individual may live in a large population with many copulation opportunities or live in almost complete isolation. Where ever freshwater pulmonates may inhabit, self-fertilization is a back-up that will always allow successful production of offspring.
Self-fertilization, however, may come at a cost. Individuals living in isolation have tendency to postpone reproduction, which in turn may lead to a decrease in the number of successful offspring produced (Auld, 2010). A study involving Biomphalaria glabrata found that even though the number of egg masses remains the same between out-crossing and self-fertilizing freshwater pulmonates, the number of eggs and successfully hatched eggs decreases with self-fertilization (Vianey-Laiud & Dussart, 2002). Inbreeding depression, the negative impact of not out-crossing genetics, occurs if a self-fertilization is used too often, allowing harmful genotypes to manifest.
Whether the eggs of an individual freshwater pulmonate are fertilized by out-crossing or self-fertilization, an egg mass is produced. After passing through a series of glands that add protective coatings and adhesives, egg mass are laid and attached to a substrate. There is one known example of brood care in the freshwater pulmonates. Protancylus, endemic to a few lakes in Indonesia, has been observed to attach its egg mass to the inside of its shell (Albrecht & Glaubrecht, 2006). After an allotted incubation period, freshwater pulmonates hatch from their eggs. Development is direct: small snails hatch and continue growing until sexual maturity is reached and the cycle begins again. Due to the wide variety of environments in which freshwater pulmonates are found, there is a great variation in the life histories strategies. Depending on the habitat, time of year, resources, etc., freshwater pulmonates may be semelparous or iteroparous. Such variations exist within species and are population dependent (Dillon, 2000).
Freshwater pulmonates have excelled at surviving in range of environments. Reproductively, simultaneous hermaphroditism, with the ability to genetically out-cross and self-fertilize, aids in the continued survival and evolution of pulmonates living in freshwater. Although a great deal is known about reproduction in simultaneously hermaphroditic freshwater pulmonates, there is always more to learn, unique circumstances to explore, and possibilities to test.
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