Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-25T23:31:54.519Z Has data issue: false hasContentIssue false
  • English
  • Français

Copulation order, density cues and variance in fertilization success in a cestode

Published online by Cambridge University Press:  20 February 2014

D. ANDREOU  and
D. P. BENESH
D. ANDREOU
Affiliation:
Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann Str. 2, Plön, D-24306, Germany School of Applied Sciences, Bournemouth University, Talbot Campus, Poole, BH12 5BB, UK
D. P. BENESH*
Affiliation:
Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann Str. 2, Plön, D-24306, Germany
*
* Corresponding author: Current address: Marine Science Institute, University of California, Santa Barbara, CA 93106-6150, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Simultaneous hermaphrodites maximize their fitness by optimizing their investment into male or female functions. Allocation of resources to male function (tissues, traits, and/or behaviours increasing paternity) is predicted to increase as density, and the associated level of sperm competition, increases. We tested whether the simultaneous hermaphroditic cestode Schistocephalus solidus uses cues of potential partner densities in its fish intermediate host to improve its male reproductive success in the final host. We had two worms, one originating from a multiple infection in the fish intermediate host and one from a single infection, sequentially compete to fertilize the eggs of a third worm. The fertilization rates of the two competitors nearly always differed from the 50–50 null expectation, sometimes considerably, implying there was a ‘winner’ in each experimental competition. However, we did not find a significant effect of density in the fish host (single vs multiple) or mating order on paternity. Additional work will be needed to identify the traits and environmental conditions that explain the high variance in male reproductive success observed in this experiment.

Keywords

copulation orderSchistocephalus solidussperm competitionsimultaneous hermaphroditesex allocationsexual selection
Type
Research Article
Information
Parasitology , Volume 141 , Issue 7 , June 2014 , pp. 934 - 939
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Al-Jahdali, M. O. (2012). Infrapopulations of Gyliauchen volubilis Nagaty, 1956 (Trematoda: Gyliauchenidae) in the rabbitfish Siganus rivulatus (Teleostei: Siganidae) from the Saudi coast of the Red Sea. Parasite 19, 227–238.CrossRefGoogle ScholarPubMed
Andris, M., Arias, M. C., Barthel, B. L., Bluhm, B. H., Bried, J., Canal, D., Chen, X. M., Cheng, P., Chiappero, M. B., Coelho, M. M., Collins, A. B., Dash, M., Davis, M. C., Duarte, M., Dubois, M.-P., Françoso, E., Galmes, M. A., Gopal, K., Jarne, P., Kalbe, M., Karczmarski, L., Kim, H., Martella, M. B., McBride, R. S., Negri, V., Negro, J. J., Newell, A. D., Piedade, A. F., Puchulutegui, C., Raggi, L., Samonte, I. E., Sarasola, J. H., See, D. R., Seyoum, S., Silva, M. C., Solaro, C., Tolley, K. A., Tringali, M. D., Vasemägi, A., Xu, L. S. and Zanón-Martínez, J. I. (2012). Permanent genetic resources added to molecular ecology resources database 1 February 2012 – 31 March 2012. Molecular Ecology Resources 12, 779–781.Google Scholar
Angeloni, L., Bradbury, J. and Charnov, E. (2002). Body size and sex allocation in simultaneously hermaphroditic animals. Behavioral Ecology 13, 419–426.Google Scholar
Anthes, N., Putz, A. and Michiels, N. K. (2006). Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework. Animal Behaviour 72, 1–12.Google Scholar
Arnold, S. and Wade, M. (1984). On the measurement of natural and sexual selection: theory. Evolution 38, 709–719.CrossRefGoogle ScholarPubMed
Avise, J. (2011). Hermaphroditism: a Primer on the Biology, Ecology, and Evolution of Dual Sexuality. Columbia University Press, New York, NY, USA.Google Scholar
Barber, I. and Scharsack, J. P. (2010). The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137, 411–424.Google Scholar
Benesh, D. P. (2013). Parental effects on the larval performance of a tapeworm in its copepod first host. Journal of Evolutionary Biology 26, 1625–1633.Google Scholar
Binz, T., Reusch, T., Wedekind, C., Schärer, L., Sternberg, J. M. and Milinski, M. (2000). Isolation and characterization of microsatellite loci from the tapeworm Schistocephalus solidus . Molecular Ecology 9, 1926–1927.Google Scholar
Birkhead, T. R. and Hunter, F. M. (1990). Mechanisms of sperm competition. Trends in Ecology and Evolution 5, 48–52.Google Scholar
Charlesworth, D. and Charlesworth, B. (1981). Allocation of resources to male and female functions in hermaphrodites. Biological Journal of the Linnean Society 15, 57–74.Google Scholar
Charnov, E. (1979). Simultaneous hermaphroditism and sexual selection. Proceedings of the National Academy of Sciences USA 76, 2480–2484.Google Scholar
Charnov, E. (1982). The theory of sex allocation. Monographs in Population Biology 18, 1–355.Google ScholarPubMed
Christen, M., Kurtz, J. and Milinski, M. (2002). Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56, 2243–2251.Google Scholar
Clarke, A. S. (1954). Studies on the life cycle of the pseudophyllidean cestode Schistocephalus solidus . Proceedings of the Zoological Society of London 124, 257–302.Google Scholar
Criscione, C. D. and Blouin, M. S. (2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212–217.Google Scholar
Criscione, C. D. and Blouin, M. S. (2006). Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evolution 60, 553–562.Google Scholar
Dörücü, M., Wilson, D. and Barber, I. (2007). Differences in adult egg output of Schistocephalus solidus from singly- and multiply-infected sticklebacks. Journal of Parasitology 93, 1518–1520.Google Scholar
Dubinina, M. N. (1980). Tapeworms (Cestoda, Ligulidae) of the Fauna of the USSR. [Translated from Russian]. Amerind Publishing Co. Pvt. Ltd., New Delhi, India.Google Scholar
Greeff, J. M., Nason, J. D. and Compton, S. G. (2001). Skewed paternity and sex allocation in hermaphroditic plants and animals. Proceedings of the Royal Society of London, Series B 268, 2143–2147.Google Scholar
Heins, D. C., Baker, J. A. and Martin, H. C. (2002). The “crowding effect” in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google Scholar
Heins, D. C., Birden, E. L. and Baker, J. A. (2010). Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus . Parasitology 137, 1681–1686.CrossRefGoogle ScholarPubMed
Heins, D. C., Baker, J. A. and Green, D. M. (2011). Processes influencing the duration and decline of epizootics in Schistocephalus solidus . Journal of Parasitology 97, 371–376.Google Scholar
Hoch, J. M. and Levinton, J. (2012). Experimental tests of sex allocation theory with two species of simultaneously hermaphroditic acorn barnacles. Evolution 66, 1332–1343.Google Scholar
Koene, J. M. and Ter Maat, A. (2007). Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite. BMC Evolutionary Biology 7, 212.Google Scholar
Lüscher, A. and Milinski, M. (2003). Simultaneous hermaphrodites reproducing in pairs self-fertilize some of their eggs: an experimental test of predictions of mixed-mating and Hermaphrodite's Dilemma. Journal of Evolutionary Biology 16, 1030–1037.Google Scholar
Lüscher, A. and Wedekind, C. (2002). Size-dependent discrimination of mating partners in the simultaneous hermaphroditic cestode Schistocephalus solidus . Behavioral Ecology 13, 254–259.Google Scholar
Nollen, P. M. (1983). Patterns of sexual reproduction among parasitic platyhelminths. Parasitology 86, 99–120.Google Scholar
Parker, G. (1990). Sperm competition games: raffles and roles. Proceedings of the Royal Society B 242, 120–126.Google Scholar
Pennycuick, L. (1971). Seasonal variations in the parasite infections in a population of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 63, 373–388.Google Scholar
Poulin, R. (2006). Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. International Journal for Parasitology 36, 877–885.Google Scholar
Schärer, L. (2009). Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63, 1377–1405.CrossRefGoogle ScholarPubMed
Schärer, L. and Ladurner, P. (2003). Phenotypically plastic adjustment of sex allocation in a simultaneous hermaphrodite. Proceedings of the Royal Society of London, Series B 270, 935–941.Google Scholar
Schärer, L. and Pen, I. (2013). Sex allocation and investment into pre-and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition. Philosophical Transactions of the Royal Society B 368, 1471–2970.Google Scholar
Schärer, L. and Wedekind, C. (1999). Lifetime reproductive output in a hermaphrodite cestode when reproducing alone or in pairs: a time cost of pairing. Evolutionary Ecology 13, 381–394.Google Scholar
Schärer, L. and Wedekind, C. (2001). Social situation, sperm competition and sex allocation in a simultaneous hermaphrodite parasite, the cestode Schistocephalus solidus . Journal of Evolutionary Biology 14, 942–953.Google Scholar
Schärer, L., Karlsson, L. M., Christen, M. and Wedekind, C. (2001). Size-dependent sex allocation in a simultaneous hermaphrodite parasite. Journal of Evolutionary Biology 14, 55–67.Google Scholar
Schjørring, S. (2009). Sex allocation and mate choice of selfed and outcrossed Schistocephalus solidus (Cestoda). Behavioral Ecology 20, 644–650.Google Scholar
Schjørring, S. and Lüscher, A. (2003). Schistocephalus solidus: a molecular test of premature gamete exchange for fertilization in the intermediate host Gasterosteus aculeatus . Experimental Parasitology 103, 174–176.CrossRefGoogle ScholarPubMed
Smyth, J. (1946). Studies on tapeworm physiology I. the cultivation of Schistocephalus solidus in vitro . Journal of Experimental Biology 23, 47–70.Google Scholar
Tan, G. N., Govedich, F. R. and Burd, M. (2004). Social group size, potential sperm competition and reproductive investment in a hermaphroditic leech, Helobdella papillornata (Euhirudinea: Glossiphoniidae). Journal of Evolutionary Biology 17, 574–580.Google Scholar
Tierney, J. and Crompton, D. (1992). Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus . Journal of Parasitology 78, 1049–1054.CrossRefGoogle Scholar
Trouvé, S., Jourdane, J., Renaud, F., Durand, P. and Morand, S. (1999). Adaptive sex allocation in a simultaneous hermaphrodite. Evolution 53, 1599–1604.Google Scholar
Van Velzen, E., Schärer, L. and Pen, I. (2009). The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites. Proceedings of the Royal Society of London, Series B 276, 3123–3131.Google Scholar
Velando, A., Eiroa, J. and Domínguez, J. (2008). Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners. Proceedings of the Royal Society of London, Series B 275, 1067–1072.Google Scholar
Wedekind, C. (1997). The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus . Parasitology 115, 317–324.Google Scholar
Wedekind, C., Strahm, D. and Schärer, L. (1998). Evidence for strategic egg production in a hermaphroditic cestode. Parasitology 117, 373–382.CrossRefGoogle Scholar
Wilson, K. and Grenfell, B. T. (1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.Google Scholar