Hostname: page-component-77c89778f8-9q27g Total loading time: 0 Render date: 2024-07-19T18:31:55.392Z Has data issue: false hasContentIssue false
  • English
  • Français

Mite choice generates sex- and size-biased infection in Drosophila hydei

Published online by Cambridge University Press:  21 March 2016

ERIN O. CAMPBELL  and
LIEN T. LUONG
ERIN O. CAMPBELL
Affiliation:
Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Building, Edmonton AB T6G 2E9, Canada
LIEN T. LUONG*
Affiliation:
Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Building, Edmonton AB T6G 2E9, Canada
*
*Corresponding author: Department of Biological Sciences, University of Alberta, CW405 Biological Sciences Buillding, Edmonton AB T6G 2E9, Canada. E-mail: lluong@ualberta.ca
Get access Rights & Permissions [Opens in a new window]

Summary

Heterogeneities in parasite infection among conspecific hosts often manifest as sex- or size-biased infections, which are typically attributed to differential host susceptibility and exposure. Since parasite fitness is often tied to host quality, host preference by parasites is likely to be under strong selection. We test the hypothesis that host preference is sufficient to generate variability in infection rate among conspecifics. Specifically, we ask whether the mite Macrocheles muscaedomesticae is able to discriminate between Drosophila hydei hosts of different sex and size, while explicitly accounting for the potential confounding effects of these two factors. Our results indicate a preference for female hosts, but this preference appears to be driven by size and not sex per se. When differences in body size were controlled for, the sex-biased infection disappeared, while mites presented with the choice of two female flies of disparate sizes were more likely to select the larger host. Across the distribution of fly body weight in this study, mites preferentially attached to flies of intermediate size. This study provides evidence that mite choice for certain host types can play an important role in parasite transmission, even in the absence of differential susceptibility or exposure among hosts.

Keywords

ectoparasitesfruit flyhost preferenceinfection heterogeneityMacrochelesparasite transmission
Type
Research Article
Information
Parasitology , Volume 143 , Issue 6 , May 2016 , pp. 787 - 793
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Allan, J. D., Flecker, A. S. and McClintock, N. L. (1987). Prey size selection by carnivorous stoneflies. Limnology and Oceanography 32, 864–872.CrossRefGoogle Scholar
Axtell, R. C. (1961). New records of North American Macrochelidae (Acarina: Mesostigmata) and their predation rates on the house fly. Annals of Entomological Society of America 54, 748.CrossRefGoogle Scholar
Axtell, R. C. (1963). Acarina occurring in domestic animal manure. Annals of Entomological Society of America 56, 628–633.CrossRefGoogle Scholar
Axtell, R. C. (1964). Phoretic relationship of some common manure-inhabiting Macrochelidae (Acarina: Mesostigmata) to the house fly. Annals of Entomological Society of America 57, 584–587.CrossRefGoogle 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
Boake, C. R. B. (1989). Correlations between courtship success, aggressive success, and body size in a picture-winged fly. Ethology 80, 318–329.CrossRefGoogle Scholar
Brandt, Y. and Andrade, M. C. B. (2007). Testing the Gravity Hypothesis of sexual size dimorphism: are smaller male faster climbers? Functional Ecology 21, 379–385.CrossRefGoogle Scholar
Campbell, K. U., Klompen, H. and Crist, T. O. (2013). The diversity and host specificity of mites associated with ants: the roles of ecological and life history traits of ant hosts. Insectes Sociaux 60, 31–41.CrossRefGoogle Scholar
Christe, P., Glaizot, O., Evanno, G., Bruyndonckx, N., Devevey, G., Yannic, G., Patthey, P., Maeder, A., Vogel, P. and Arlettaz, R. (2007). Host sex and ectoparasites choice: preference for, and higher survival on female hosts. Journal of Animal Ecology 76, 703–710.CrossRefGoogle ScholarPubMed
Dallas, T. and Foré, S. (2013). Chemical attraction of Dermacentor variabilis ticks to Peromyscus leucopus based on host body mass and sex. Experimental and Applied Acarology 61, 243–250.CrossRefGoogle ScholarPubMed
Daralova, A., Hoi, H. and Schleicher, B. (1997). The effect of ectoparasite nest load on the breeding biology of the Penduline Tit Remiz pendulinus . Ibis 139, 115–120.CrossRefGoogle Scholar
Duffy, M. A., Brassil, C. E., Hall, S. R., Tessier, A. J., Cáceres, C. E. and Conner, J. K. (2008). Parasite-mediated disruptive selection in a natural Daphnia population. BMC Evolutionary Biology 8, 80. doi: 10.1186/1471-2148-8-80.CrossRefGoogle Scholar
Dye, C. and Hasibeder, G. (1986). Population-dynamics of mosquito-borne disease: effects of flies which bite some people more frequently than others. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 69–77.CrossRefGoogle ScholarPubMed
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
Gilburn, A. S., Stewart, K. M. and Edward, D. A. (2009). Sex-biased phoretic mite load on two seaweed flies: Coelopa frigida and Coelopa pilipes . Environmental Entomology 38, 1608–1612.CrossRefGoogle ScholarPubMed
Gonzalez-Santoyo, I. and Cordoba-Aguilar, A. (2012). Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata 142, 1–16.CrossRefGoogle Scholar
Grossman, J. D. and Smith, R. J. (2008). Phoretic mite discrimination among male burying beetle (Nicrophorus investigator) hosts. Annals of the Entomological Society of America 101, 266–271.CrossRefGoogle Scholar
Grutter, A. S. and Poulin, R. (1998). Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Marine Ecology Progress Series 164, 263–271.CrossRefGoogle Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites. Science 218, 382–387.CrossRefGoogle Scholar
Harrison, J. F., Camazine, S., Marden, J. H., Kirkton, S. D., Rozo, A. and Yang, X. (2001). Mite not makes it home: tracheal mites reduce the safety margin for oxygen delivery of flying honeybees. The Journal of Experimental Biology 204, 805–814.CrossRefGoogle ScholarPubMed
Honěk, A. (1993). Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66, 483–492.CrossRefGoogle Scholar
Iliadi, K. G., Iliadi, N. N., Rashkovetsky, E. L., Girin, S. V., Nevo, E. and Korol, A. B. (2002). Sexual differences for emigration behavior in natural populations of Drosophila melanogaster . Behavior Genetics 32, 173–180.CrossRefGoogle ScholarPubMed
Jalil, M. and Rodriguez, J. G. (1970). Studies of behaviour of Macrocheles muscaedomesticae (Acarina: Macrochelidae) with emphasis on its attraction to the house fly. Annals of the Entomological Society of America 63, 738–744.CrossRefGoogle Scholar
Johnston, J. S. and Templeton, A. R. (1982). Dispersal and clines in Opuntia breeding Drosophila mercatorum and Drosophila hydei at Kamuela, Hawaii. In Ecological Genetics and Evolution: the Cactus-Yeast-Drosophila Model System (ed. Barker, J. S. F. and Starmer, W. T.), pp. 241–256. Academic Press, Sydney.Google Scholar
Kiffner, C., Stanko, M., Morand, S., Khokhlova, I. S., Shenbrot, G. I., Laudisoit, A., Leirs, H., Hawlena, H. and Krasnov, B. R. (2013). Sex-biased parasitism is not universal: evidence from rodent-flea associations from three biomes. Oecologia 173, 1009–1022.CrossRefGoogle Scholar
Krantz, G. W. (1988). Reflections on the biology, morphology and ecology of the Macrochelidae. Experimental and Applied Acarology 22, 125–137.CrossRefGoogle Scholar
Krasnov, B. R., Bordes, F., Khokhlova, I. S. and Morand, S. (2012). Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76, 1–13.CrossRefGoogle Scholar
Krishnan, A., Muralidharan, S., Sharma, L. and Borges, R. M. (2010). A hitchhiker's guide to a crowded syconium: how do fig nematodes find the right ride? Functional Ecology, 24, 741–749.CrossRefGoogle Scholar
Lajeunesse, M. J., Forbes, M. R. and Smith, B. P. (2004). Species and sex biases in ectoparasitism of dragonflies by mites. Oikos 106, 501–508.CrossRefGoogle Scholar
Lefranc, A. and Bundgaard, J. (2000). The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster . Hereditas 132, 243–247.CrossRefGoogle ScholarPubMed
Luong, L. T., Heath, B. D. and Polak, M. (2007). Host inbreeding increases susceptibility to ectoparasitism. Journal of Evolutionary Biology 20, 79–86.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Niogret, J., Lumaret, J. P. and Bertrand, M. (2006). Semiochemicals mediating host-finding behaviour in the phoretic association between Macrocheles saceri (Acari : Mesostigmata) and Scarabaeus species (Coleoptera : Scarabaeidae). Chemoecology 16, 129–134.CrossRefGoogle Scholar
Pastorok, R. A. (1981). Prey vulnerability and size selection by Chaoborus larvae. Ecology 62, 1311–1324.CrossRefGoogle Scholar
Polak, M. (1996). Ectoparasitic effects on host survival and reproduction: the Drosophila–Macrocheles association. Ecology 77, 1379–1389.CrossRefGoogle Scholar
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147, 287–295.CrossRefGoogle Scholar
R Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ Google Scholar
Robertson, F. W. (1957). Studies of quantitative inheritance XI. Genetic and environmental correlation between body size and egg production in Drosophila melanogaster . Journal of Genetics 55, 428–443.CrossRefGoogle Scholar
Rodrigueiro, T. S. C. and Prado, A. P. (2004). Macrocheles muscaedomesticae (Acari, Macrochelidae) and a species of Uroseius (Acari, Polyaspididae) phoretic on Musca domestica (Diptera, Muscidae): effects on dispersal and colonization of poultry manure. Iheringia, Serie Zoologia 94, 181–185.CrossRefGoogle Scholar
Roger, C., Coderre, D. and Boivin, G. (2000). Differential prey utilization by the generalist predator Coleomegilla maculata lengi according to prey size and species. Entomologia Experimentalis et Applicata 94, 3–13.CrossRefGoogle Scholar
Rózsa, L. (1997). Wing feather mite (Acari: Proctophyllodidae) abundance correlates with body mass of passerine hosts: a comparative study. Canadian Journal of Zoology-Revue Canadienne De Zoologie 75, 1535–1539.CrossRefGoogle Scholar
Sabelis, M. W. (1992). Predatory arthropods. In Natural Enemies. The Population Biology of Predators, Parasites and Diseases (ed. Crawley, M.), pp. 225–264. Blackwell, Oxford.CrossRefGoogle Scholar
Schalk, G. and Forbes, M. R. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67–74.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133.CrossRefGoogle ScholarPubMed
Sivinski, J. M. and Dodson, G. (1992). Sexual dimorphism in Anastrepha suspensa (Loew) and other tephritid fruit-flies (Diptera, Tephritidae) – possible roles of developmental rate, fecundity, and dispersal. Journal of Insect Behavior 5, 491–506.CrossRefGoogle Scholar
Soroker, V., Nelson, D. R., Bahar, O., Reneh, S., Yablonski, S. and Palevsky, E. (2003). Whitefly wax as a cue for phoresy in the broad mite, Polyphagotarsonemus latus (Acari : Tarsonemidae). Chemoecology 13, 163–168.CrossRefGoogle Scholar
Valera, F., Hoi, H., Daralova, 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
Wade, C. F. and Rodriguez, J. G. (1961). Life history of Machrocheles muscaedomesticae (Acarina: Macrochelidae), a predator of the house fly. Annals of Entomological Society of America 54, 776–781.CrossRefGoogle Scholar
Williams, D. F. and Rogers, A. J. (1976). Vertical and lateral distribution of stable flies in northwestern Florida. Journal of Medical Entomology 13, 95–98.CrossRefGoogle ScholarPubMed
Wilson, K., Bjornstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolf, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Disease (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford.CrossRefGoogle 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.CrossRefGoogle Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.CrossRefGoogle ScholarPubMed