Parthenogenesis in populations of Campeloma decisum (Gastropoda: Viviparidae)
by Caitlin M. Luebke
BIOL/WATER 361, Fall 2013
Parthenogenesis is an asexual reproductive mode that does not require fertilization for embryos to development. The offspring produced by parthenogenesis are genetically identical to their maternal genotypes. Parthenogenesis occurs mostly in plants and invertebrate species. One invertebrate species that has been found to exhibit parthenogenesis is Campeloma decisum (Gastropoda: Viviparidae). C. decisum is a useful model organism for studying parthenogenesis because both parthenogenetic and sexual populations have been found to exist throughout its distribution. By examining the various current hypotheses as to the causes and maintenance of parthenogenesis in some populations of C. decisum, we can learn more about the evolution of this reproductive mode.
It is important to know more about Campeloma decisum in order to understand the current hypotheses behind its reproductive modes. C. decisum is an ovoviviparous, freshwater snail that inhabits lentic and lotic ecosystems of eastern North America (Johnson, 1992a) This prosobranch snail is a deposit feeder on fine detritus and is a significant food source for many fish and diving ducks (Van Appledorn et al., 2007). C. decisum is an intermediate host for several parasites. One such parasite is Leucochloridiomorpha constantiae (Trematoda: Brachylaemidae). According Johnson (1994) L. constantiae is a parasitic, digenetic trematode that is found as an unencysted larva within the female’s brood chamber. When a female snail is infected, this trematode is thought to either consume the sperm cells that enter her brood chamber or block the sperm from reaching her eggs. Once a female is infected with L. constantiae it is not possible for her to recover. This parasitic behavior is thought to be responsible for the occurrence and/or the maintenance of parthenogenesis in some populations of C. decisum. There are several other hypotheses as to the causes and maintenance of parthenogenesis in populations of C. decisum. Throughout this discussion, it is important to remember that these hypotheses are still being studied and are not necessarily mutually exclusive of one another.
There are currently three main hypotheses to explain the cause of parthenogenesis in Campeloma decisum. As mentioned previously, larval Leucochloridiomorpha constantiae limit sperm for the female. One hypothesis is that infected female populations evolved to be able to reproduce asexually (i.e. parthenogenesis) as a direct response to this parasitism. This hypothesis can be observed in the findings of Johnson (1992a). Johnson found that once L. constantiae is introduced into a sexual population, sperm is severely limited which results in selection for parthenogenesis. Another hypothesis to explain the cause of parthenogenesis in C. decisum is that parthenogenesis appeared spontaneously through genetic mutation. In Johnson’s study (1992b), genetic variation at 19 enzyme loci were analyzed for individuals from 18 different C. decisum populations. The results showed that some parthenogenetic populations were found to be homozygous at all loci. This discovery leads us to believe that these parthenogenetic populations occur spontaneously because homozygosity for these loci is not found in the sexual populations. The third hypothesis to explain the cause of parthenogenesis in C. decisum is addressed in the same study conducted by Johnson (1992b). This hypothesis states that parthenogenesis arose by the hybridization of genetically distinct sexual ancestors. Johnson’s results also showed that there are some parthenogenetic populations that are heterozygous for the same loci. This discovery leads us to believe that parthenogenesis can also occur by means of hybridization of sexual linages. Although there are several current hypotheses to explain the cause of parthenogenesis in C. decisum, it is important to remember that more than one of these hypotheses may be correct. Now that we examined the current hypotheses to explain the cause of parthenogenesis in C. decisum, we must look at the current hypotheses for how parthenogenesis is retained.
There are currently four main hypotheses as to how parthenogenesis is maintained in certain populations of Campeloma decisum. The first hypothesis suggests that parthenogenesis is actually maintained by the presence of Leucochloridiomorpha constantiae by its strong sterility selection against males, as previously mentioned. This hypothesis is very similar to the hypothesis that explains the cause of parthenogenesis which can be observed in the findings of Johnson (1992a). The second hypothesis is that the maintenance of parthenogenesis is a reflection of its advantageous ability to safeguard against competitors and parasites (Lively, 1992). In the case of C. decisum parthenogenesis protects the species from dwindling due to the sperm-limiting, parasitic trematode (Johnson, 1992a). The third hypothesis is known as reproductive assurance. This hypothesis says that parthenogenesis is favored in sparse populations where male density is low. The reproductive assurance hypothesis can be observed in the findings of (Lively, 1992). Lively found that the frequency of parthenogenetic populations is higher in northern, glaciated regions than in southern, unglaciated regions. Northern, glaciated regions had an overall sparser population of C. decisum than the southern, unglaciated regions. The fourth hypothesis is known as the Red Queen. The Red Queen hypothesis was first proposed by Leigh Van Valen in 1973. Its name refers to a statement made by the Red Queen in Lewis Carroll’s 1871 novel entitled, “Through the Looking-Glass.” In the story, the Red Queen tells Alice, “Now, here, you see, it takes all the running you can do, to keep in the same place.” Van Valen used this quote as the basis for the Red Queen hypothesis. This hypothesis says that organisms must constantly evolve and adapt to a changing environment in order to survive. The Red Queen hypothesis is often applied to predator/prey and parasite/host relationships. According to Johnson (1994), the Red Queen hypothesis can be interpreted as saying that there is a negative correlation between the rate of parasitism and sexual reproduction. In other words, L. constantiae is scarce in sexual populations because C. decisum is constantly evolving to resist the trematode. This causes us to believe that parthenogenetic populations experience a higher rate of parasitism than sexual populations because parthenogenetic populations are unable to constantly evolve. This can be observed in the findings of Johnson (1994). Johnson found that all parthenogenetic populations of C. decisum were infected with L. constantiae while no sexual populations were infected. Johnson’s results tell us that snail reproductive mode is not independent of the presence of L. constantiae. Further support for the Red Queen hypothesis can be found in the results of Lively (1992). Lively observed that parthenogenesis is maintained in northern, glaciated regions because there is a low-density of parasites in these areas. If an organism inhabits an area with few parasites, they are not involved in an &ldqquo;arms race” and do not necessarily need resistant genotypes. In this case, asexual reproduction (e.g. parthenogenesis) could be adequate. Just as with the hypotheses that explain the cause of parthenogenesis, more than one hypothesis may explain its maintenance.
Now that the current hypotheses regarding the cause and maintenance of parthenogenesis have been examined, we can evaluate the advantages and disadvantages of parthenogenesis. Reproducing by means of parthenogenesis has several advantages. As previously mentioned, parthenogenesis is advantageous to Campeloma decisum because it protects populations from dwindling due to the sperm-limiting behavior of Leucochloridiomorpha constantiae. Parthenogenesis is also much more efficient than sex. The ability to produce offspring without a partner eliminates the expenditure of energy on mating behaviors. In addition, parthenogenesis allows reproduction to occur in situations where there is an absence or a low-density of suitable males. Although parthenogenesis has some advantages, there are also some significant disadvantages to reproducing asexually. As previously discussed, sexual reproduction is often selected over asexual reproduction because it allows populations to produce resistant genotypes as protection against parasites. Parthenogenetic populations are thus more susceptible to parasites because they are unlikely to produce these resistant genotypes. This can be observed in the findings of Johnson (1994). Johnson found that there is a higher prevalence of parasitism in parthenogenetic populations than sexual populations. It can be assumed that parthenogenetic populations are also more susceptible to disease than sexual reproducing populations.
Campeloma decisum is an excellent model organism for studying the evolution of parthenogenesis because both parthenogenetic and sexual populations exist within its distribution. By studying this snail, biologists have been able to develop several hypotheses to explain the cause and maintenance of this reproductive mode. Although we are not sure which hypotheses (if any) are correct, we can attempt to propose several possible evolutionary histories of parthenogenesis in C. decisum by piecing together the existing theories. Parthenogenesis may have occurred spontaneously by the means of a genetic mutation and is maintained by the sperm-limiting behavior of Leucochloridiomorpha constantiae. Or perhaps parthenogenesis was first caused by L. constantiae and is preserved by idea that northern populations have a low density of males. Maybe parthenogenesis was caused by hybridization and spontaneous mutation and is maintained by the Red Queen hypothesis. There are many current possible explanations for the occurrence and maintenance of parthenogenesis within C. decisum and each one sheds a little light on the mysterious evolution of this reproductive strategy. Further studies might want to ask questions that relate to how these two reproductive modes are affecting the C. decisum population as a whole. Do the parthenogenetic populations and sexual populations differ in ways other than reproductive strategies? Would these differences result in speciation? What would happen if C. decisum were introduced to an exotic environment or controlled setting? Would sexual reproduction be retained or would parthenogenesis occur again? There are still many more unanswered questions. With any luck, however, future studies of parthenogenesis in C. decisum will allow researchers to adhere to the Red Queen theory and evolve their hypotheses according to new discoveries so that we can better understand the evolution of not only parthenogenesis but also reproduction in general.
- Johnson, S.G. 1992a. Parasite-induced parthenogenesis in a freshwater snail: stable, persistent patterns of parasitism. Oecologia 89: 533-541.
- Johnson, S.G. 1992b. Spontaneous and hybrid origins of parthenogenesis in Campeloma decisum (freshwater prosobranch snail). Heredity 68: 253-261.
- Johnson, S.G. 1994. Parasitism, reproductive assurance and the evolution of reproduction mode in a freshwater snail. Proceedings: Biological Sciences 255: 209-213.
- Lively, C.M. 1992. Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution 46(4): 907-913.
- Van Appledorn, M., D.A. Lamb, K. Albalak & C.E. Bach. 2007. Zebra mussels decrease burrowing ability and growth of a native snail, Campeloma decisum. Hydrobiologia 575: 441-445.