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Parasite performance and host alternation: is there a negative effect in host-specific and host-opportunistic parasites?

Published online by Cambridge University Press:  27 March 2017

LUTHER VAN DER MESCHT ,
IRINA S. KHOKHLOVA ,
ELIZABETH M. WARBURTON  and
BORIS R. KRASNOV
LUTHER VAN DER MESCHT*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 8499000 Midreshet Ben-Gurion, Israel Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990 Midreshet Ben-Gurion, Israel
IRINA S. KHOKHLOVA
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990 Midreshet Ben-Gurion, Israel
ELIZABETH M. WARBURTON
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 8499000 Midreshet Ben-Gurion, Israel
BORIS R. KRASNOV
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 8499000 Midreshet Ben-Gurion, Israel
*
*Corresponding author: Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. E-mail: vanderme@post.bgu.ac.il
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Summary

Environmental fluctuations are expected to require special adaptations only if they are associated with a decrease in fitness. We compared reproductive performance between fleas fed on alternating (preferred and non-preferred) hosts and fleas fed solely on either a preferred or a non-preferred host to determine whether (1) host alternation incurs an immediate negative effect, and, if yes, then (2) whether this effect is greater in a host specialist (Parapulex chephrenis) than in host generalists (Xenopsylla conformis and Synosternus cleopatrae). We also compared flea performance under alternating host regimes with different host order (initial feeding on either a preferred or a non-preferred host). An immediate negative effect of alternating hosts on reproductive performance was found in P. chephrenis only. These fleas produced 44·3% less eggs that were 3·6% smaller when they fed on alternating hosts as compared with a preferred host. In contrast, X. conformis and S. cleopatrae appeared to be able to adapt their reproductive strategy to host alternation by producing higher quality offspring (on average, 3·1% faster development and 2·1% larger size) without compromising offspring number. However, the former produced eggs that were slightly, albeit significantly, smaller when it fed on alternating hosts as compared with a preferred host. Moreover, host order affected reproductive performance in host generalists (e.g. 2·8% larger eggs when the first feeding was performed on a non-preferred host), but not in a host specialist. We conclude that immediate effects of environmental fluctuation on parasite fitness depend on the degree of host specialization.

Keywords

host alternationenvironmental fluctuationflearodents
Type
Research Article
Information
Parasitology , Volume 144 , Issue 8 , July 2017 , pp. 1107 - 1116
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Berrigan, D. (1991). The allometry of egg size and number in insects. Oikos 60, 31–21.Google Scholar
Bonnet, X., Naulleau, G., Shine, R. and Lourdais, O. (2001). Short-term versus long-term effects of food intake on reproductive output in a viviparous snake, Vipera aspis . Oikos 92, 297–308.Google Scholar
Boyce, M. S. and Daley, D. J. (1980). Population tracking of fluctuating environments and natural selection for tracking ability. American Naturalist 115, 480–491.CrossRefGoogle Scholar
Brooks, D. R. and Hoberg, E. P. (2007). How will global climate change affect parasite–host assemblages? Trends in Parasitology 23, 571–574.CrossRefGoogle ScholarPubMed
Brooks, D. R., León-Règagnon, V., McLennan, D. A. and Zelmer, D. (2006). Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87, S76–S85.Google Scholar
Buckling, A., Brockhurst, M. A., Travisano, M. and Rainey, P. B. (2007). Experimental adaptation to high and low quality environments under different scales of temporal variation. Journal of Evolutionary Biology 20, 296–300.Google Scholar
Chapman, C. A., Gillespie, T. R. and Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology 14, 134–144.CrossRefGoogle Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Day, J. F. and Benton, A. H. (1980). Population dynamics and coevolution of adult siphonapteran parasites of the southern flying squirrel (Glaucomys volans volans). American Midland Naturalist 103, 333–338.Google Scholar
Fielden, L. J., Krasnov, B. and Khokhlova, I. (2001). Respiratory gas exchange in the flea Xenopsylla conformis (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 735–739.Google Scholar
Fielden, L. J., Krasnov, B. R., Khokhlova, I. S., and Arakelyan, M. S. (2004). Respiratory gas exchange in the desert flea Xenopsylla ramesis (Siphonaptera: Pulicidae): response to temperature and blood-feeding. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 137, 557–565.CrossRefGoogle ScholarPubMed
Filimonova, S. A. (1986). Changes in the ultra-structure of the intestinal epithelium of Xenopsylla cheopis (Siphonaptera) after emerging from cocoons and beginning of feeding. Parazitologiya 20, 99–105 in Russian.Google Scholar
Fischer, K. and Fiedler, K. (2001). Egg weight variation in the butterfly Lycaena hippothoe: more small or fewer large eggs? Population Ecology 43, 105–109.Google Scholar
Fox, C. W. (1993). The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae). Oecologia 96, 139–146.Google Scholar
Fox, C. W., Thakar, M. S. and Mousseau, T. A. (1997). Egg size plasticity in a seed beetle: an adaptive maternal effect. American Naturalist 149, 149–163.Google Scholar
Garcίa-Barros, E. (1992). Evidence for geographic variation of egg size and fecundity in a satyrine butterfly, Hipparchia semele (L.) (Lepidoptera-Nymphalidae-Satyrinae). Graellsia 48, 45–52.Google Scholar
Gavrilets, S. and Scheiner, S. M. (1993). The genetics of phenotypic plasticity. VI. Theoretical predictions for directional selection. Journal of Evolutionary Biology 6, 49–68.Google Scholar
Giron, D. and Casas, J. (2003). Mothers reduce egg provisioning with age. Ecology Letters 6, 273–277.Google Scholar
Harvey, G. T. (1983 a). A geographical cline in egg weights in Choristoneura fumiferana (Lepidoptera: Tortricidae) and its significance in population dynamics. Canadian Entomologist 115, 1103–1108.CrossRefGoogle Scholar
Harvey, G. T. (1983 b). Environmental and genetic effects on mean egg weight in spruce budworm (Lepidoptera: Tortricidae). Canadian Entomologist 115, 1109–1117.Google Scholar
Hothorn, T., Bretz, F. and Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.CrossRefGoogle ScholarPubMed
Janzen, D. H. (1985). On ecological fitting. Oikos 45, 308–310.Google Scholar
Kassen, R. (2002). The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15, 173–190.Google Scholar
Kelly, C. K. and Horning, K. (1999). Acquisition order and resource value in Cuscuta attenuata . Proceedings of the Natural Academy of Sciences of the United States of America 96, 13219–13222.Google Scholar
Khokhlova, I. S., Ghazaryan, L., Krasnov, B. R. and Degen, A. A. (2008). Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent infesting fleas. Functional Ecology 22, 530–536.CrossRefGoogle Scholar
Khokhlova, I. S., Serobyan, V., Degen, A. A. and Krasnov, B. R. (2010). Host gender and offspring quality in a flea parasitic on a rodent. Journal of Experimental Biology 213, 3299–3304.CrossRefGoogle Scholar
Khokhlova, I. S., Fielden, L. J., Degen, A. A. and Krasnov, B. R. (2012). Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters. Journal of Evolutionary Biology 25, 2005–2013.Google Scholar
Khokhlova, I. S., Fielden, L. J., Williams, J. B., Degen, A. A. and Krasnov, B. R. (2013). Energy expenditure for egg production in arthropod ectoparasites: the effect of host species. Parasitology 140, 1070–1077.Google Scholar
Kiefer, D., Warburton, E. M., Khokhlova, I. S. and Krasnov, B. R. (2016). Reproductive consequences of female size in haematophagous ectoparasites. Journal of Experimental Biology 219, 2368–2376.Google Scholar
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khokhlova, I. S. (1997). Host-habitat relation as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159–173.Google Scholar
Krasnov, B. R., Hastriter, M., Medvedev, S. G., Shenbrot, G. I., Khokhlova, I. S. and Vatschenok, V. S. (1999) Additional records of fleas (Siphonaptera) on wild rodents in the southern part of Israel. Israel Journal of Zoology 45, 333–340.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001 a). The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629–637.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001 b). Development rates of two Xenopsylla flea species in relation to air temperature and humidity. Medical and Veterinary Entomology 15, 249–258.Google Scholar
Krasnov, B. R., Burdelov, S. A., Khokhlova, I. S. and Burdelova, N. V. (2003 a). Sexual size dimorphism, morphological traits and jump performance in seven species of desert fleas (Siphonaptera). Journal of Zoology London 261, 181–189.CrossRefGoogle Scholar
Krasnov, B. R., Khokhlova, I. S., and Shenbrot, G. I. (2003 b). Density-dependent host selection in ectoparasites: an application of isodar theory to fleas parasitizing rodents. Oecologia 134, 365–372.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Burdelova, N. V., Mirzoyan, N. S. and Degen, A. A. (2004 a). Fitness consequences of host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. Journal of Animal Ecology 73, 815–820.Google Scholar
Krasnov, B. R., Poulin, R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. (2004 b). Ectoparasitic “jacks-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. American Naturalist 164, 506–516.Google Scholar
Krasnov, B. R., Burdelova, N. V., Khokhlova, I. S., Shenbrot, G. I. and Degen, A. A. (2005 a). Pre-imaginal interspecific competition in two flea species parasitic on the same rodent host. Ecological Entomology 30, 146–155.Google Scholar
Krasnov, B. R., Poulin, R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. (2005 b). Host specificity and geographic range in haematophagous ectoparasites. Oikos 108, 449–456.Google Scholar
Krasnov, B. R., Korine, C., Burdelova, N. V., Khokhlova, I. S. and Pinshow, B. (2007). Between-host phylogenetic distance and feeding efficiency in hematophagous ectoparasites: rodent fleas and a bat host. Parasitology Research 101, 365.Google Scholar
Lawrence, W. and Foil, L. D. (2002). The effect of diet upon pupal development and cocoon formation by the cat flea (Siphonaptera: Pulicidae). Journal of Vector Ecology 27, 39–43.Google Scholar
Magalhães, S., Cailleau, A., Blanchet, E. and Olivieri, I. (2014). Do mites evolving in alternating host plants adapt to host switch? Journal of Evolutionary Biology 27, 1956–1964.Google Scholar
McIntyre, G. S. and Gooding, R. H. (2000). Egg size, contents, and quality: maternal-age and -size effects on house fly eggs. Canadian Journal of Zoology 78, 1544–1551.Google Scholar
Martin, T. E. (1987). Food as a limit on breeding birds: a life-history perspective. Annual Review of Ecology and Systematics 18, 453–487.Google Scholar
Nuismer, S. L. and Thompson, J. N. (2006). Coevolutionary alternation in antagonistic interactions. Evolution 60, 2207–2217.Google Scholar
Packer, M. J. and Corbet, P. S. (1989). Size variation and reproductive success of female Aedes punctor (Diptera: Culicidae). Ecological Entomology 14, 297–309.CrossRefGoogle Scholar
Parker, G. A. and Begon, M. (1986). Optimal egg size and clutch size – effects of environment and maternal phenotype. American Naturalist 128, 573–592.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and R Core Team (2016). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–128, http://CRAN.R-project.org/package=nlme.Google Scholar
Poulin, R. (1998) Large-scale patterns of host use by parasites of freshwater fishes. Ecology Letters 1, 118–128.Google Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763–776.Google Scholar
Pöykkö, H. and Mänttäri, S. (2012). Egg size and composition in an ageing capital breeder – consequences for offspring performance. Ecological Entomology 37, 330–341.Google Scholar
R Development Core Team (2015). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.Google Scholar
Reboud, X. and Bell, G. (1997). Experimental evolution in Chlamydomonas. 3. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78, 507–514.CrossRefGoogle Scholar
Sutherland, W. (1996). From Individual Behaviour to Population Ecology (Oxford Series in Ecology and Evolution). Oxford University Press, Oxford, UK.Google Scholar
Torres-Vila, L. M., and Rodríguez-Molina, M. C. (2002). Egg size variation and its relationship with larval performance in the Lepidoptera: the case of the European grapevine moth Lobesia botrana . Oikos 99, 272–283.Google Scholar
Venail, P. A., Kaltz, O., Olivieri, I., Pommier, T. and Mouquet, N. (2011). Diversification in temporally heterogeneous environments: effect of the grain in experimental bacterial populations. Journal of Evolutionary Biology 24, 2485–2495.Google Scholar
Ward, S. A. (1992). Assessing functional explanations of host specificity. American Naturalist 139, 883–891.Google Scholar
Williams, T. D. (1994). Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biological Reviews 68, 35–59.Google Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host–parasite interactions. Trends in Parasitology 25, 236–244.Google Scholar