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Fecundity compensation and fecundity reduction among populations of the three-spined stickleback infected by Schistocephalus solidus in Alaska

Published online by Cambridge University Press:  28 April 2014

DAVID C. HEINS  and
JOHN A. BAKER
DAVID C. HEINS*
Affiliation:
Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, Louisiana 70118, USA Department of Biology, Clark University, Worcester, Massachusetts 01610, USA
JOHN A. BAKER
Affiliation:
Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, Louisiana 70118, USA Department of Biology, Clark University, Worcester, Massachusetts 01610, USA
*
* Corresponding author: Department of Ecology and Evolutionary Biology, 400 Lindy Boggs Center, Tulane University, New Orleans, Louisiana 70118, USA. E-mail: [email protected]
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Summary

We surveyed nine populations of the three-spined stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus from south-central Alaska for two apparent forms of tolerance to infection in females capable of producing egg clutches notwithstanding large parasite burdens. Seven populations exhibited fecundity reduction, whereas two populations showed fecundity compensation. Our data suggest that fecundity reduction, a side effect resulting from nutrient theft, occurs in two phases of host response influenced by the parasite : host body mass (BM) ratio. The first is significantly reduced ovum mass without significant reduction in clutch size, and the second one involves significant reductions in both ovum mass and clutch size. Thus, ovum mass of host females who are functionally being starved through nutrient theft seems to be more readily influenced by parasitism and, therefore, decreased before clutch size is reduced. This inference is consistent with expectations based on the biology of and effect of feeding ration on reproduction in stickleback females. Fecundity compensation appears to be uncommon among populations of three-spined stickleback in Alaska and rare among populations throughout the northern hemisphere. Fecundity reduction seems to be common, at least among stickleback populations in Alaska.

Keywords

Castrationclutch sizefecundity compensationfecundity reductionparasitismSchistocephalus solidusthree-spined sticklebacktolerancetrade-offreproduction
Type
Research Article
Information
Parasitology , Volume 141 , Issue 8 , July 2014 , pp. 1088 - 1096
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Agnew, P., Koella, J. C. and Michalakis, Y. (2000). Host life history responses to parasitism. Microbes and Infection 2, 891–896.CrossRefGoogle ScholarPubMed
Ali, M. and Wootton, R. J. (1999). Effect of variable food levels on reproductive performance of breeding female three-spined sticklebacks. Journal of Fish Biology 55, 1040–1053.Google Scholar
Arme, C. and Owen, R. W. (1967). Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects. Parasitology 57, 301–314.CrossRefGoogle ScholarPubMed
Ayres, J. S. and Schneider, D. S. (2012). Tolerance of infections. Annual Review of Immunology 30, 271–294.CrossRefGoogle ScholarPubMed
Baker, J. A., Foster, S. A., Heins, D. C., Bell, M. A. and King, R. W. (1998). Variation in female life-history traits among Alaskan populations of the three-spined stickleback, Gasterosteus aculeatus L. (Pisces: Gasterosteidae). Biological Journal of the Linnean Society 63, 141–159.Google Scholar
Bakker, T. C. M. and Mundwiler, B. (1994). Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population. Behavioral Ecology 5, 74–80.CrossRefGoogle Scholar
Barber, I. (2013). Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends in Parasitology 29, 556–566.CrossRefGoogle ScholarPubMed
Baucom, R. S. and de Roode, J. C. (2011). Ecological immunology and tolerance in plants and animals. Functional Ecology 25, 18–28.CrossRefGoogle Scholar
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–352.CrossRefGoogle ScholarPubMed
Brown-Peterson, N. J. and Heins, D. C. (2009). Interspawning interval of wild female three-spined stickleback Gasterosteus aculeatus in Alaska. Journal of Fish Biology 74, 2299–2312.CrossRefGoogle ScholarPubMed
de Roij, J., Harris, P. D. and MacColl, D. C. (2011). Divergent resistance to a monogenean flatworm among three-spined stickleback populations. Functional Ecology 25, 217–226.CrossRefGoogle Scholar
Fletcher, D. A. (1984). Effects of food supply on egg quality and quantity in fishes. Ph.D. thesis. University of Wales, Aberystwyth, Wales, UK.Google Scholar
Fletcher, D. A. and Wootton, R. J. (1995). A hierarchical response to differences in ration size in the reproductive performance of female three-spined sticklebacks. Journal of Fish Biology 46, 657–668.Google Scholar
Fogelman, R. M., Kuris, A. M. and Grutter, A. S. (2009). Parasitic castration of a vertebrate: effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinal fish, Cheilodipterus quinquelineatus . International Journal for Parasitology 39, 577–583.CrossRefGoogle Scholar
Granovitch, A. I., Yagunova, E. B., Maximovich, A. N. and Sokolova, I. M. (2009). Elevated female fecundity as a possible compensatory mechanism in response to trematode infestation in populations of Littorina saxatilis (Olivi). International Journal for Parasitology 39, 1011–1019.CrossRefGoogle ScholarPubMed
Hall, S. R., Becker, C. and Cáceres, C. E. (2007). Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295–309.CrossRefGoogle Scholar
Heins, D. C. (2012). Fecundity compensation in the three-spined stickleback Gasterosteus aculeatus infected by the diphyllobothriidean cestode Schistocephalus solidus . Biological Journal of the Linnean Society 106, 807–819.CrossRefGoogle Scholar
Heins, D. C. and Baker, J. A. (1993). Clutch production in the darter Etheostoma lynceum Hay and its implications for life history study. Journal of Fish Biology 42, 819–829.Google Scholar
Heins, D. C. and Baker, J. A. (2003). Reduction in egg size in natural populations of three-spined stickleback infected with a cestode macroparasite. Journal of Parasitology 89, 1–6.CrossRefGoogle Scholar
Heins, D. C. and Baker, J. A. (2008). The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625–645.CrossRefGoogle Scholar
Heins, D. C. and Brown-Peterson, N. J. (2010). Influence of the pseudophyllidean cestode Schistocephalus solidus on oocyte development in three-spined stickleback Gasterosteus aculeatus . Parasitology 137, 1151–1158.CrossRefGoogle Scholar
Heins, D. C., Singer, S. S. and Baker, J. A. (1999). Virulence of the cestode Schistocephalus solidus and reproduction in infected three-spined stickleback, Gasterosteus aculeatus . Canadian Journal of Zoology 77, 1967–1974.CrossRefGoogle Scholar
Heins, D. C., Baker, J. A., Toups, M. A. and Birden, E. L. (2010 a). Evolutionary significance of fecundity reduction in three-spined stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus . Biological Journal of the Linnean Society 100, 835–846.CrossRefGoogle Scholar
Heins, D. C., Birden, E. L. and Baker, J. A. (2010 b). 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.CrossRefGoogle ScholarPubMed
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.CrossRefGoogle ScholarPubMed
Krist, A. C. (2001). Variation in fecundity among populations of snails is predicted by prevalence of castrating parasites. Evolutionary Ecology Research 3, 191–197.Google Scholar
Kuris, A. M. (2003). Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89, S96–S100.Google Scholar
Lafferty, K. D. and Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17, 507–513.CrossRefGoogle Scholar
LoBue, C. P. and Bell, M. A. (1993). Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the three-spined stickleback. American Naturalist 142, 725–735.CrossRefGoogle Scholar
McPhail, J. D. and Peacock, S. D. (1983). Some effects of the cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus): evolutionary aspects of a host-parasite interaction. Canadian Journal of Zoology 61, 901–908.CrossRefGoogle Scholar
Medzhitov, R., Schneider, D. S. and Soares, M. P. (2012). Disease tolerance as a defense strategy. Science 335, 936–941.CrossRefGoogle ScholarPubMed
Milinski, M. (1990). Parasites and host decision-making. In Parasitism and Host Behavior (ed. Barnard, C. J. and Behnke, J. M.), pp. 95–116. Taylor & Francis, London, UK.Google Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
Minchella, D. J. and LoVerde, P. T. (1981). A cost of increased early reproductive effort in the snail Biomphalaria glabrata . American Naturalist 118, 876–881.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, New York, NY, USA.CrossRefGoogle Scholar
Parker, B. J., Barribeau, S. M., Laughton, A. M., de Roode, J. C. and Gerardo, N. M. (2011). Non-immunological defense in an evolutionary framework. Trends in Ecology and Evolution 26, 242–248.CrossRefGoogle Scholar
Pennycuick, L. (1971). Quantitative effects of three species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus . Journal of Zoology, London 165, 143–162.CrossRefGoogle Scholar
Polak, M. and Starmer, W. T. (1998). Parasite-induced risk of mortality elevates reproductive effort in male Drosophila . Proceedings of the Royal Society of London Series B: Biological Sciences 265, 2197–2201.CrossRefGoogle ScholarPubMed
Råberg, L., Graham, A. L. and Read, A. F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 364, 37–49.CrossRefGoogle ScholarPubMed
Reist, J. D. (1985). An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Canadian Journal of Zoology 63, 1429–1439.CrossRefGoogle Scholar
Scharsack, J. P., Kalbe, M., Harrod, C. and Gisep, R. (2007). Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proceedings of the Royal Society of London Series B: Biological Sciences 274, 1523–1532.Google ScholarPubMed
Schultz, E. T., Topper, M. and Heins, D. C. (2006). Decreased reproductive investment of female three-spined stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect? Oikos 114, 303–310.CrossRefGoogle Scholar
Simms, E. L. (2000). Defining tolerance as a norm of reaction. Evolutionary Ecology 14, 563–570.CrossRefGoogle Scholar
Smith, V. (2007). Host resource supplies influence the dynamics and outcome of infectious disease. Integrative and Comparative Biology 47, 310–316.CrossRefGoogle ScholarPubMed
Sullivan, L. M. and D'Agostino, R. B. Sr. (2002). Robustness and power of analysis of covariance applied to data distorted from normality by floor effects: non-homogeneous regression slopes. Journal of Statistical Computation and Simulation 72, 141–165.CrossRefGoogle Scholar
Svensson, E. I. and Råberg, L. (2010). Resistance and tolerance in animal enemy – victim coevolution. Trends in Ecology and Evolution 25, 267–274.CrossRefGoogle ScholarPubMed
Tierney, J. F., Huntingford, F. A. and Crompton, D. W. T. (1996). Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology 49, 483–493.Google Scholar
Williams, G. C. (1966). Adaptation and Natural Selection. Princeton University Press, Princeton, NJ, USA.Google Scholar
Woods, P. F. (1985). Limnology of Nine Small Lakes, Matanuska-Susitna Borough, Alaska, and the Survival and Growth Rates of Rainbow Trout. United States Geological Survey Water Resources Investigative Report 85–4292. Geological Survey, United States Department of the Interior, Anchorage, AK, USA.Google Scholar
Wootton, R. J. (1973). The effect of size of food ration on egg production in the female three-spined stickleback, Gasterosteus aculeatus L. Journal of Fish Biology 5, 89–96.CrossRefGoogle Scholar
Wootton, R. J. (1976). The Biology of the Sticklebacks. Academic Press, London, UK.Google Scholar
Wootton, R. J. (1977). Effect of food limitation during the breeding season on the size, body components and egg production of female sticklebacks (Gasterosteus aculeatus). Journal of Animal Ecology 46, 823–834.CrossRefGoogle Scholar
Wootton, R. J. (1994). Energy allocation in the threespine stickleback. In The Evolutionary Biology of the Threespine Stickleback (ed. Bell, M. A. and Foster, S. A.), pp. 114–143. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Wu, Y. B. (1984). The effects of heterogeneous regression slopes on the robustness of two test statistics in the analysis of covariance. Educational and Psychological Measurement 44, 647–663.CrossRefGoogle Scholar