Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T09:22:18.417Z Has data issue: false hasContentIssue false
  • English
  • Français

State-dependent parasitism by a facultative parasite of fruit flies

Published online by Cambridge University Press:  23 June 2017

LIEN T. LUONG ,
TAYLOR BROPHY ,
EMILY STOLZ  and
SOLOMON J. CHAN
LIEN T. LUONG*
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9, Canada
TAYLOR BROPHY
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9, Canada
EMILY STOLZ
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9, Canada
SOLOMON J. CHAN
Affiliation:
Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9, Canada
*
*Corresponding author: Department of Biological Sciences, CW405 Biological Sciences Bldg., University of Alberta, Edmonton, AB T6G 2E9, Canada. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Parasites can evolve phenotypically plastic strategies for transmission such that a single genotype can give rise to a range of phenotypes depending on the environmental condition. State-dependent plasticity in particular can arise from individual differences in the parasite's internal state or the condition of the host. Facultative parasites serve as ideal model systems for investigating state-dependent plasticity because individuals can exhibit two life history strategies (free-living or parasitic) depending on the environment. Here, we experimentally show that the ectoparasitic mite Macrocheles subbadius is more likely to parasitize a fruit fly host if the female mite is mated; furthermore, the propensity to infect increased with the level of starvation experienced by the mite. Host condition also played an important role; hosts infected with moderate mite loads were more likely to gain additional infections in pairwise choice tests than uninfected flies. We also found that mites preferentially infected flies subjected to mechanical injury over uninjured flies. These results suggest that a facultative parasite's propensity to infect a host (i.e. switch from a free-living strategy) depends on both the parasite's internal state and host condition. Parasites often live in highly variable and changing environments, an infection strategy that is plastic is likely to be adaptive.

Keywords

aggregationectoparasiteDrosophilaMacrochelesmitephenotypic plasticityhost preferencestate-dependent behaviour
Type
Research Article
Information
Parasitology , Volume 144 , Issue 11 , September 2017 , pp. 1468 - 1475
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science 294, 321–326.CrossRefGoogle ScholarPubMed
Bedhomme, S., Agnew, P., Sidobre, C. and Michalakis, Y. (2004). Virulence reaction norms across a food gradient. Proceedings of the Royal Society B-Biological Sciences 271, 739–744. doi: 10.1098/rspb.2003.2657.Google Scholar
Beresford, D. V. and Sutcliffe, J. F. (2009). The effect of Macrocheles muscaedomesticase and M. subbadius (Acarina: Macrochelidae) phoresy on the dispersal of Stomoxys calcitrans (Diptera: Muscidae). Systematic and Applied Acarology Special Publications 23, 1–30.Google Scholar
Bonte, D., Van Dyck, H., Bullock, J. M., Coulon, A., Delgado, M., Gibbs, M., Lehouck, V., Matthysen, E., Mustin, K., Saastamoinen, M., Schtickzelle, N., Stevens, V. M., Vandewoestijne, S., Baguette, M., Barton, K., Benton, T. G., Chaput-Bardy, A., Clobert, J., Dytham, C., Hovestadt, T., Meier, C. M., Palmer, S. C. F., Turlure, C. and Travis, J. M. J. (2012). Costs of dispersal. Biological Reviews 87, 290–312. doi: 10.1111/j.1469-185X.2011.00201.x.Google Scholar
Brown, S. P., Cornforth, D. M. and Mideo, N. (2012). Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends in Microbiology 20, 336–342. doi: 10.1016/j.tim.2012.04.005.Google Scholar
Buckling, A. G. J., Taylor, L. H., Carlton, J. M. R. and Read, A. F. (1997). Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proceedings of the Royal Society B-Biological Sciences 264, 553–559.Google Scholar
Campbell, E. O. and Luong, L. T. (2016). Mite choice generates sex- and size-biased infection in Drosophila hydei . Parasitology 143, 787–793. doi: 10.1017/s0031182016000305.CrossRefGoogle ScholarPubMed
Cornet, S., Bichet, C., Larcombe, S., Faivre, B. and Sorci, G. (2014). Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. Journal of Animal Ecology 83, 256–265. doi: 10.1111/1365-2656.12113.Google Scholar
Dhooria, M. S. (2016). Fundamentals of Applied Acarology. Springer Science+Business Media, Singapore.Google Scholar
Farish, D. J. and Axtell, R. C. (1971). Phoresy redefined and examined in Macrocheles muscaedomesticae (Acari: Macrochelidae). Acarologia 13, 16–29.Google Scholar
Fenton, A. and Rands, S. A. (2004). Optimal parasite infection strategies: a state-dependent approach. International Journal for Parasitology 34, 813–821. doi: 10.1016/j.ijpara.2004.02.003.Google Scholar
Filipponi, A. (1964). Experimental taxonomy applied to the Macrochelidae (Acari: Mesotigmata). In Proceedings of the First International Congress of Acarology (ed. Evans, G. O.), 92–100. Acarologia, Paris.Google Scholar
Fordyce, J. A. (2006). The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. Journal of Experimental Biology 209, 2377–2383.Google Scholar
Genovart, M., Negre, N., Tavecchia, G., Bistuer, A., Parpal, L. and Oro, D. (2010). The young, the weak and the sick: evidence of natural selection by predation. PLoS ONE 5, e9774. doi: 10.1371/journal.pone.0009774.Google Scholar
Ghalambor, C. K., McKay, J. K., Carroll, S. P. and Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394–407. doi: 10.1111/j.1365-2435.2007.01283.x.Google Scholar
Glass, E. V., Yoder, J. A. and Needham, G. R. (1998). Clustering reduces water loss by adult American house dust mites Dermatophagoides farinae (Acari: Pyroglyphidae). Experimental & Applied Acarology 22, 31–37. doi: 10.1023/a:1006081323887.Google Scholar
Harrison, A., Scatlebury, M. and Montgomery, W. I. (2010). Body mass and sex-biased parasitism in wood mice Apodmeus sylvaticus . Oikos 199, 1099–1104.Google Scholar
Harrison, J. F., Woods, H. A. and Roberts, S. P. (2012). Ecological and Environmental Physiology of Insects. Oxford Univ. Press, New York.CrossRefGoogle Scholar
Hess, E. and Decastro, J. J. (1986). Field tests of the response of female Amblyomma variegatum (Acari, Ixodidae) to the synthetic aggregation-attachment pheromone and its components. Experimental & Applied Acarology 2, 249–255. doi: 10.1007/bf01193957.Google Scholar
Houston, A. I. and McNamara, J. M. (1992). Phenotypic plasticity as a state-dependent life-history decision. Evolutionary Ecology 6, 243–253. doi: 10.1007/bf02214164.Google Scholar
Houston, A. I. and McNamara, J. M. (1999). Models of Adaptive Behaviour: An Approach Based on State. Cambridge University Press Cambridge, UK.Google Scholar
Kaltz, O. and Koella, J. C. (2003). Host growth conditions regulate the plasticity of horizontal and vertical transmission in Holospora undulata, a bacterial parasite of the protozoan Paramecium caudatum . Evolution 57, 1535–1542. doi: 10.1554/02-635.Google ScholarPubMed
Luong, L. T., Heath, B. D. and Polak, M. (2007). Host inbreeding increases susceptibility to ectoparasitism. Journal of Evolutionary Biology 20, 79–86. doi: 10.1111/j.1420-9101.2006.01226.x.Google Scholar
Luong, L. T., Penoni, L. R., Horn, C. J. and Polak, M. (2015). Physical and physiological costs of ectoparasitic mites on host flight endurance. Ecological Entomology 40, 518–524. doi: 10.1111/een.12218.Google Scholar
Mathot, K. J. and Dall, S. R. X. (2013). Metabolic rates can drive individual differences in information and insurance use under the risk of starvation. American Naturalist 182, 611–620. doi: 10.1086/673300.CrossRefGoogle ScholarPubMed
Mideo, N. and Reece, S. E. (2012). Plasticity in parasite phenotypes: evolutionary and ecological implications for disease. Future Microbiology 7, 17–24. doi: 10.2217/fmb.11.134.Google Scholar
Norval, R. A. I., Andrew, H. R. and Yunker, C. E. (1989). Pheromone-mediation of host-selection in bont ticks (Amblyomma hebraeum Koch). Science 243, 364–365.Google Scholar
Pigliucci, M. (2001). Phenotypic Plasticity: Beyond Nature and Nurture. The John Hopkins University Press, Baltimore.CrossRefGoogle Scholar
Polak, M. (1996). Ectoparasitic effects on host survival and reproduction: the Drosophila-Macrocheles association. Ecology 77, 1379–1389.CrossRefGoogle Scholar
Polak, M. and Markow, T. A. (1995). Effect of ectoparasitic mites on sexual selection in a Sonoran desert fruit fly. Evolution 49, 660–669.Google Scholar
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 2899–2903.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, New Jersey.Google Scholar
Powers, K. S. and Aviles, L. (2003). Natal dispersal patterns of a subsocial spider Anelosimus cf. jucundus (Theridiidae). Ethology 109, 725–737. doi: 10.1046/j.1439-0310.2003.00918.x.Google Scholar
R Development Core Team (2015). R: A language and environment for statistical computing. In R Foundation for Statistical Computing Vienna, Austria. http://www.R-project.org/.Google Scholar
Reece, S. E., Ramiro, R. S. and Nussey, D. H. (2009). Plastic parasites: sophisticated strategies for survival and reproduction? Evolutionary Applications 2, 11–23. doi: 10.1111/j.1752-4571.2008.00060.x.Google Scholar
Restif, O. and Kaltz, O. (2006). Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite. Oikos 114, 148–158.Google Scholar
Ruf, D., Dorn, S. and Mazzi, D. (2011). Females leave home for sex: natal dispersal in a parasitoid with complementary sex determination. Animal Behaviour 81, 1083–1089. doi: 10.1016/j.anbehav.2011.02.028.Google Scholar
Schlichting, C. and Pigliucci, M. (1998). Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates Inc., Sunderland, MA.Google Scholar
Sih, A., Mathot, K. J., Moiron, M., Montiglio, P. O., Wolf, M. and Dingemanse, N. J. (2015). Animal personality and state-behaviour feedbacks: a review and guide for empiricists. Trends in Ecology & Evolution 30, 50–60. doi: 10.1016/j.tree.2014.11.004.Google Scholar
Stankowich, T. (2003). Marginal predation methodologies and the importance of predator preferences. Animal Behaviour 66, 589–599. doi: 10.1006/anbe.2003.2232.Google Scholar
Stasiuk, S. J., Scott, M. J. and Grant, W. N. (2012). Developmental plasticity and the evolution of parasitism in an unusual nematode, Parastrongyloides trichosuri . Evodevo 3, 14. doi: 10.1186/2041-9139-3-1.CrossRefGoogle Scholar
Taylor, P. D., Day, T., Nagy, D., Wild, G., Andre, J. B. and Gardner, A. (2006). The evolutionary consequences of plasticity in host-pathogen interactions. Theoretical Population Biology 69, 323–331. doi: 10.1016/j.tpb.2005.09.004.Google Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387–390. doi: 10.1016/s1471-4922(02)02339-5.Google Scholar
Tseng, M. (2006). Interactions between the parasite's previous and current environment mediate the outcome of parasite infection. American Naturalist 168, 565–571. doi: 10.1086/507997.CrossRefGoogle ScholarPubMed
Valera, F., Hoi, H., Darolova, A. and Kristofik, J. (2004). Size versus health as a cue for host choice: a test of the tasty chick hypothesis. Parasitology 129, 59–68.CrossRefGoogle Scholar
Van Oosten, A. R., Matthysen, E. and Heylen, D. J. A. (2016). The more the merrier – experimental evidence for density-dependent feeding facilitation in the bird-specialised tick Ixodes arboricola . International Journal for Parasitology 46, 187–193. doi: 10.1016/j.ijpara.2015.11.002.CrossRefGoogle ScholarPubMed
Vizoso, D. B. and Ebert, D. (2005). Phenotypic plasticity of host-parasite interactions in response to the route of infection. Journal of Evolutionary Biology 18, 911–921. doi: 10.1111/j.1420-9101.2005.00920.x.Google Scholar
Walter, D. E. and Proctor, H. C. (2013). Mites: Ecology, Evolution, and Behavior. Oxford University Press, New York.Google Scholar
Wang, H., Hails, R. S., Cui, W. W. and Nuttall, P. A. (2001). Feeding aggregation of the tick Rhipicephalus appendiculatus (Ixodidae): benefits and costs in the contest with host responses. Parasitology, 123, 447–453. doi: 10.1017/s0031182001008654.Google Scholar
Wertheim, B., van Baalen, E. J. A., Dicke, M. and Vet, L. E. M. (2005). Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. In Annual Review of Entomology, Vol. 50, pp. 321–346. Annual Reviews, Palo Alto.Google Scholar
West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20, 249–278.Google Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236–244. doi: 10.1016/j.pt.2009.02.004.Google Scholar
Zhang, Z. Q. (1991). Parasitism of Acyrthosiphon pisum by Allothrombium pulvinum (Acariformes, Trombidiidae) – host attachment site, host size selection, superparasitism and effect on host. Experimental & Applied Acarology 11, 137–147. doi: 10.1007/bf01246086.Google Scholar