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The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity

Published online by Cambridge University Press:  09 October 2003

H. M. FERGUSON ,
A. RIVERO  and
A. F. READ
H. M. FERGUSON
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
A. RIVERO
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK Present address: CNRS (Centre d'Etudes sur le Polymorphisme des Microorganismes), IRD, 911 avenue Agropolis, 34394, Montpellier Cedex 5, France.
A. F. READ
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
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Abstract

Studies of invertebrate–parasite interactions frequently report that infection reduces host fecundity. The extent of the reduction is likely to be determined by a wide range of host and parasite factors. We conducted a laboratory experiment to evaluate the role of parasite genetics and infection genetic diversity on the fecundity of mosquitoes carrying malaria parasites. The malaria vector Anopheles stephensi was infected with either of 2 different genotypes of the rodent malaria parasite Plasmodium chabaudi, or by a mixture of both. Mixed genotype infections reduced mosquito fecundity by 20%, significantly more than either of the 2 single genotype infections. Mixed genotype infections were associated with high gametocyte densities and anaemia in mice, both of which were correlated with reduced bloodmeal size in mosquitoes. Bloodmeal size was the most important predictor of mosquito fecundity; the presence and number of parasites had no direct effect. Parasite density influenced the propensity of mosquitoes to feed on infected mice, with a higher percentage of mosquitoes taking a meal as asexual parasite and gametocyte density increased. Thus mosquitoes may preferentially feed on hosts who will most impair their fecundity.

Keywords

Plasmodium chabaudimosquitoesmalariafecunditygenetic diversityfeeding behaviour
Type
Research Article
Information
Parasitology , Volume 127 , Issue 1 , July 2003 , pp. 9 - 19
Copyright
2003 Cambridge University Press

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References

REFERENCES

AHMED, A. M., MAINGON, R. D., TAYLOR, P. J. & HURD, H. (1999). The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae. Invertebrate Reproduction and Development 36, 217–222.CrossRefGoogle Scholar
ARIEY, F., CHALVET, W., HOMMEL, D., PENEAU, C., HULIN, A., MERCEREAUPUIJALON, O., DUCHEMIN, J. B., SARTHOU, J. L., REYNES, J. M. & FANDEUR, T. (1999). Plasmodium falciparum parasites in French Guiana: limited genetic diversity and high selfing rate. American Journal of Tropical Medicine and Hygiene 61, 978–985.CrossRefGoogle Scholar
BABIKER, H. A., RANFORD-CARTWRIGHT, L. C., CURRIE, D., CHARLWOOD, J. D., BILLINGSLEY, P., TEUSCHER, T. & WALLIKER, D. (1994). Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109, 413–421.CrossRefGoogle Scholar
BAYLIS, M. & MBWABI, A. (1995). Feeding-behavior of tsetse-flies (Glossina pallidipes austen) on trypanosoma-infected oxen in Kenya. Parasitology 110, 297–305.CrossRefGoogle Scholar
BEALE, G. H., CARTER, R. & WALLIKER, D. ( 1978). Genetics. In Rodent Malaria (ed. Killick-Kendrick, R. & Peters, W.) Academic Press, London.CrossRef
BRAKS, M. A. H., ANDERSON, R. A. & KNOLS, B. G. J. (1999). Infochemicals in mosquito host selection: human skin microflora and Plasmodium parasites. Parasitology Today 15, 409–413.CrossRefGoogle Scholar
BRIEGEL, H. (1980). Determination of uric acid and hematin in a single sample of excreta from blood-fed insects. Experientia 36, 1428.CrossRefGoogle Scholar
BRIEGEL, H. (1990 a). Fecundity, metabolism, and body size in Anopheles (Diptera, Culicidae), vectors of malaria. Journal of Medical Entomology 27, 839–850.Google Scholar
BRIEGEL, H. (1990 b). Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. Journal of Insect Physiology 36, 165–172.Google Scholar
BURKOT, T., NARARA, A., PARU, R., GRAVES, P. & GARNER, P. (1989). Human host selection by anophelines: no evidence of preferential selection of malaria or microfilariae-infected individuals in a hyperendemic area. Parasitology 98, 337–342.CrossRefGoogle Scholar
CARWARDINE, S. L. & HURD, H. (1997). Effects of Plasmodium yoelii nigeriensis infection on Anopheles stephensi egg development and resorption. Medical and Veterinary Entomology 11, 265–269.CrossRefGoogle Scholar
COLEMAN, R. E. & EDMAN, J. D. (1988). Feeding site selection of Lutzomyia longipalpis (Diptera, Psychodidae) on mice infected with Leishmania mexicana amazonensis. Journal of Medical Entomology 25, 229–233.CrossRefGoogle Scholar
COLEMAN, R. E., EDMAN, J. D. & SEMPREVIVO, L. H. (1988). Interactions between malaria (Plasmodium yoelii) and Leishmaniasis (Leishmania mexicana amazonensis) – effect of concomitant infection on host activity, host body temperature, and vector engorgement success. Journal of Medical Entomology 25, 467–471.CrossRefGoogle Scholar
DAY, J. F., EBERT, K. M. & EDMAN, J. D. (1983). Feeding patterns of mosquitoes (Diptera, Culicidae) simultaneously exposed to malarious and healthy mice, including a method for separating blood meals from conspecific hosts. Journal of Medical Entomology 20, 120–127.CrossRefGoogle Scholar
DAY, J. F. & EDMAN, J. D. (1983). Malaria renders mice susceptible to mosquito feeding when gametocytes are most infective. Journal of Parasitology 69, 163–170.CrossRefGoogle Scholar
DAY, J. F. & EDMAN, J. D. (1984). The importance of disease induced changes in mammalian body- temperature to mosquito blood feeding. Comparative Biochemistry and Physiology 77, 447–452.CrossRefGoogle Scholar
FERDIG, M. T., BEERNTSEN, B. T., SPRAY, F. J., LI, J. & CHRISTENSEN, B. M. (1993). Reproductive costs associated with resistance in a mosquito-filarial worm system. American Journal of Tropical Medicine and Hygiene 49, 756–762.CrossRefGoogle Scholar
FERGUSON, H. M. & READ, A. F. (2002). Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proceedings of the Royal Society of London, B 269, 1217–1224.CrossRefGoogle Scholar
FRANK, S. A. (1992). A kin selection model for the evolution of virulence. Proceedings of the Royal Society of London, B 250, 195–197.CrossRefGoogle Scholar
FRANK, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78.CrossRefGoogle Scholar
FREIER, J. E. & FRIEDMAN, S. (1976). Effect of host infection with Plasmodium gallinaceum on the reproductive capacity of Aedes aegypti. Journal of Invertebrate Pathology 28, 161–166.CrossRefGoogle Scholar
GRAVES, P. M., CARTER, R. & McNEILL, K. M. (1984). Gametocyte production in cloned lines of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 33, 1045–1050.CrossRefGoogle Scholar
GROSSMAN, G. L. & PAPPAS, L. G. (1991). Human skin temperature and mosquito (Diptera: Culicidae) blood feeding rate. Journal of Medical Entomology 28, 456–460.CrossRefGoogle Scholar
HACKER, C. S. (1971). The differential effect of Plasmodium gallinaceum on the fecundity of several strains of Aedes aegypti. Journal of Invertebrate Pathology 18, 373–377.CrossRefGoogle Scholar
HACKER, C. S. & KILAMA, W. L. (1974). The relationship between Plasmodium gallinaceum density and fecundity of Aedes aegypti. Journal of Invertebrate Pathology 23, 101–105.CrossRefGoogle Scholar
HOGG, J. C. & HURD, H. (1995 a). Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Medical and Veterinary Entomology 9, 176–180.Google Scholar
HOGG, J. C. & HURD, H. (1995 b). Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111, 555–562.Google Scholar
HOGG, J. C. & HURD, H. (1997). The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s.l. in north east Tanzania. Parasitology 114, 325–331.Google Scholar
HURD, H. (1998). Parasite manipulation of insect reproduction: who benefits? Parasitology 116, S13–S21.Google Scholar
HURD, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.Google Scholar
HOSOI, T. (1959). Identification of blood components which induce gorging of the mosquito. Journal of Insect Physiology 3, 191–218.CrossRefGoogle Scholar
JAHAN, N. & HURD, H. (1997). The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of Anopheles stephensi. Annals of Tropical Medicine and Parasitology 91, 365–369.CrossRefGoogle Scholar
JAHAN, N. & HURD, H. (1998). Effect of Plasmodium yoelii nigeriensis (Haemosporidia: Plasmodiidae) on Anopheles stephensi (Diptera: Culicidae) vitellogenesis. Journal of Medical Entomology 35, 956–961.CrossRefGoogle Scholar
JAMES, S. P., NICOL, W. D. & SHUTE, P. G. (1932). Clinical and parasitological observations on induced malaria. Proceedings of the Royal Society of Medicine 25, 879–893.Google Scholar
MACKINNON, M., GAFFNEY, D. & READ, A. (2002). Virulence of malaria parasites: host genotype by parasite genotype interactions. Infection, Genetics, and Evolution 36, 1–10.Google Scholar
MACKINNON, M. J. & READ, A. F. (1999 a). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689–703.Google Scholar
MACKINNON, M. J. & READ, A. F. (1999 b). Selection for high and low virulence in the malaria parasite Plasmodium chabaudi. Proceedings of the Royal Society of London, B 266, 741–748.Google Scholar
MAHON, R. & GIBBS, A. ( 1982). Arbovirus-infected hens attract more mosquitoes. In Viral Diseases in Southeast Asia and the Western Pacific (ed Mackenzie, J. D.), pp. 502–504. Academic Press, Sydney.
MORET, Y. & SCHMID-HEMPEL, P. (2000). Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.CrossRefGoogle Scholar
OFOSU-OKYERE, A., MACKINNON, M. J., SOWA, M. P., KORAM, K. A., NKRUMAH, F., OSEI, Y. D., HILL, W. G., WILSON, M. D. & ARNOT, D. E. (2001). Novel Plasmodium falciparum clones and rising clone multiplicities are associated with the increase in malaria morbidity in Ghanaian children during the transition into the high transmission season. Parasitology 123, 113–123.CrossRefGoogle Scholar
PENN, D. & POTTS, W. K. (1998). Chemical signals and parasite-mediated sexual selection. Trends in Ecology and Evolution 13, 391–396.CrossRefGoogle Scholar
READ, A. F. & TAYLOR, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle Scholar
REISEN, W. K. & EMORY, R. W. (1976). Blood feeding of Anopheles stephensi. Annals of the Entomological Society of America 69, 293–298.CrossRefGoogle Scholar
ROSSIGNOL, P. A., RIBEIRO, J. M. C., JUNGERY, M., TURELL, M. J., SPIELMAN, A. & BAILEY, C. L. (1985). Enhanced mosquito blood-finding success on parasitemic hosts – evidence for vector parasite mutualism. Proceedings of the National Academy of Sciences, USA 82, 7725–7727.CrossRefGoogle Scholar
ROWE, J. A., MOULDS, J. M., NEWBOLD, C. I. & MILLER, L. H. (1997). P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature, London 388, 292–295.Google Scholar
SAS, I. I. (1997). SAS/STAT Software: Changes and Enhancements through Release 6.12. SAS Institute Inc, Cary, NC.
SASAKI, A. & IWASA, Y. (1991). Optimal growth schedule of pathogens within a host: switching between lytic and latent cycles. Theoretical Population Biology 39, 201–239.CrossRefGoogle Scholar
SHIEH, J. N. & ROSSIGNOL, P. A. (1992). Opposite influences of host anemia on blood feeding rate and fecundity of mosquitos. Parasitology 105, 159–163.CrossRefGoogle Scholar
SRIKRISHNARAJ, K. A., RAMASAMY, R. & RAMASAMY, M. S. (1993). Fecundity of Anopheles tessellatus reduced by the ingestion of murine anti-mosquito antibodies. Medical and Veterinary Entomology 7, 66–68.CrossRefGoogle Scholar
TAKKEN, W. & KNOLS, B. G. J. (1999). Odor-mediated behavior of Afrotropical malaria mosquitoes. Annual Review of Entomology 44, 131–157.CrossRefGoogle Scholar
TAYLOR, L. H., MACKINNON, M. J. & READ, A. F. (1998). Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi. Evolution 52, 583–591.CrossRefGoogle Scholar
TAYLOR, P. J. & HURD, H. (2001). The influence of host haematocrit on the blood feeding success of Anopheles stephensi: implications for enhanced malaria transmission. Parasitology 122, 491–496.CrossRefGoogle Scholar
TIMMS, R., COLEGRAVE, N., CHAN, B. H. K. & READ, A. F. (2001). The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 123, 1–11.CrossRefGoogle Scholar
TURELL, M. J., BAILEY, C. L. & ROSSI, C. (1984). Increased mosquito feeding on Rift Valley fever virus-infected lambs. American Journal of Tropical Medicine and Hygiene 33, 1232–1238.CrossRefGoogle Scholar
VAN BAALEN, M. & SABELIS, M. W. (1995). The dynamics of multiple infection and the evolution of virulence. American Naturalist 146, 881–910.CrossRefGoogle Scholar