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Malaria Journal
Published in: Malaria Journal 1/2011

Open Access 01-12-2011 | Research

Maternal environment shapes the life history and susceptibility to malaria of Anopheles gambiae mosquitoes

Authors: Lena M Lorenz, Jacob C Koella

Published in: Malaria Journal | Issue 1/2011

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Abstract

Background

It is becoming generally recognized that an individual's phenotype can be shaped not only by its own genotype and environmental experience, but also by its mother's environment and condition. Maternal environmental factors can influence mosquitoes' population dynamics and susceptibility to malaria, and therefore directly and indirectly the epidemiology of malaria.

Methods

In a full factorial experiment, the effects of two environmental stressors - food availability and infection with the microsporidian parasite Vavraia culicis - of female mosquitoes (Anopheles gambiae sensu stricto) on their offspring's development, survival and susceptibility to malaria were studied.

Results

The offspring of A. gambiae s.s. mothers infected with V. culicis developed into adults more slowly than those of uninfected mothers. This effect was exacerbated when mothers were reared on low food. Maternal food availability had no effect on the survival of their offspring up to emergence, and microsporidian infection decreased survival only slightly. Low food availability for mothers increased and V. culicis-infection of mothers decreased the likelihood that the offspring fed on malaria-infected blood harboured malaria parasites (but neither maternal treatment influenced their survival up to dissection).

Conclusions

Resource availability and infection with V. culicis of A. gambiae s.s. mosquitoes not only acted as direct environmental stimuli for changes in the success of one generation, but could also lead to maternal effects. Maternal V. culicis infection could make offspring more resistant and less likely to transmit malaria, thus enhancing the efficacy of the microsporidian for the biological control of malaria.
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Literature
1.
Rogers DJ, Randolph SE: The global spread of malaria in a future, warmer world. Science. 2000, 289: 1763-1766.CrossRefPubMed
2.
Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M: Malaria resurgence in the East African highlands: Temperature trends revisited. Proc Natl Acad Sci USA. 2006, 103: 5829-5834. 10.1073/pnas.0508929103.PubMedCentralCrossRefPubMed
3.
Gilioli G, Mariani L: Sensitivity of Anopheles gambiae population dynamics to meteo-hydrological variability: a mechanistic approach. Malar J. 2011, 10: 294-10.1186/1475-2875-10-294.PubMedCentralCrossRefPubMed
4.
Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB: Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA. 2010, 107: 15135-15139. 10.1073/pnas.1006422107.PubMedCentralCrossRefPubMed
5.
Mousseau TA, Dingle H: Maternal effects in insect life histories. Annu Rev Entomol. 1991, 36: 511-534. 10.1146/annurev.en.36.010191.002455.CrossRef
6.
7.
Otti O, Sadd BM: Parental guidance? Trans-generational influences on offspring life history in mosquitoes. Trends Parasitol. 2008, 24: 197-199. 10.1016/j.pt.2008.02.004.CrossRefPubMed
8.
Mousseau TA, Fox CW: The adaptive significance of maternal effects. Trends Ecol Evol. 1998, 13: 403-407. 10.1016/S0169-5347(98)01472-4.CrossRefPubMed
9.
Prasad NG, Shakarad M, Rajamani M, Joshi A: Interaction between the effects of maternal and larval levels of nutrition on pre-adult survival in Drosophila melanogaster. Evol Ecol Res. 2003, 5: 903-911.
10.
Grech K, Maung LA, Read AF: The effect of parental rearing conditions on offspring life history in Anopheles stephensi. Malaria J. 2007, 6: 130139-CrossRef
11.
Rossiter MC: Incidence and consequences of inherited environmental effects. Annu Rev Ecol Syst. 1996, 27: 451-476. 10.1146/annurev.ecolsys.27.1.451.CrossRef
12.
Jones TM, Widemo F: Survival and reproduction when food is scarce: Implications for a lekking Hawaiian Drosophila. Ecol Entomol. 2005, 30: 397-405. 10.1111/j.0307-6946.2005.00705.x.CrossRef
13.
Kyneb A, Toft S: Effects of maternal diet quality on offspring performance in the rove beetle Tachyporus hypnorum. Ecol Entomol. 2006, 31: 322-330. 10.1111/j.1365-2311.2006.00775.x.CrossRef
14.
Miller GA, Pell JK, Simpson SJ: Crowded locusts produce hatchlings vulnerable to fungal attack. Biol Letters. 2009, 5: 845-848. 10.1098/rsbl.2009.0495.CrossRef
15.
Frost PC, Ebert D, Larson JH, Marcus MA, Wagner ND, Zalewski A: Transgenerational effects of poor elemental food quality on Daphnia magna. Oecologia. 2010, 162: 865-872. 10.1007/s00442-009-1517-4.CrossRefPubMed
16.
Mitchell SE, Read AF: Poor maternal environment enhances offspring disease resistance in an invertebrate. Proc R Soc London, B. 2005, 272: 2601-2607. 10.1098/rspb.2005.3253.CrossRef
17.
Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J: Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J Anim Ecol. 2010, 79: 403-413. 10.1111/j.1365-2656.2009.01617.x.CrossRefPubMed
18.
Little TJ, Kraaijeveld AR: Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol. 2004, 19: 58-60. 10.1016/j.tree.2003.11.011.CrossRefPubMed
19.
Moret Y, Schmid-Hempel P: Entomology - Immune defence in bumble-bee offspring. Nature. 2001, 414: 506-506.CrossRefPubMed
20.
Freitak D, Heckel DG, Vogel H: Dietary-dependent trans-generational immune priming in an insect herbivore. Proc R Soc London, B. 2009, 276: 2617-2624. 10.1098/rspb.2009.0323.CrossRef
21.
Brown MJF, Loosli R, Schmid-Hempel P: Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos. 2000, 91: 421-427. 10.1034/j.1600-0706.2000.910302.x.CrossRef
22.
Bedhomme S, Agnew P, Sidobre C, Michalakis Y: Virulence reaction norms across a food gradient. Proc R Soc London, B. 2004, 271: 739-744. 10.1098/rspb.2003.2657.CrossRef
23.
Fellous S, Koella JC: Cost of co-infection controlled by infectious dose combinations and food availability. Oecologia. 2010, 162: 935-940. 10.1007/s00442-009-1535-2.CrossRefPubMed
24.
Vàvra J, Becnel JJ: Vavraia culicis (Weiser, 1947) Weiser, 1977 revisited: Cytological characterisation of a Vavraia culicis-like microsporidium isolated from mosquitoes in Florida and the establishment of Vavraia culicis floridensis subsp n. Folia Parasitol (Praha). 2007, 54: 259-271.CrossRef
25.
Lorenz LM, Koella JC: The microsporidian parasite Vavraia culicis as a potential late-life acting control agent of malaria. Evol Appl. 2011, 4: 783-790. 10.1111/j.1752-4571.2011.00199.x.PubMedCentralCrossRefPubMed
26.
Koella JC, Lynch PA, Thomas MB, Read AF: Towards evolution-proof malaria control with insecticides. Evol Appl. 2009, 2: 469-480. 10.1111/j.1752-4571.2009.00072.x.PubMedCentralCrossRefPubMed
27.
Bargielowski I, Koella JC: A possible mechanism for the suppression of Plasmodium berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia culicis. PLoS One. 2009, 4: e4676-10.1371/journal.pone.0004676.PubMedCentralCrossRefPubMed
28.
Agnew P, Becnel JJ, Ebert D, Michalakis Y: Symbiosis of microsporidia and insects. Insect Symbiosis. Edited by: Bourtzis K, Miller T. 2003, Boca Raton, FL: CRC Press, 2: 145-163.
29.
Bradshaw WE, Johnson K: Initiation of metamorphosis in the pitcher-plant mosquito: Effects of larval growth history. 1995, 76: 2055-2065.
30.
Mendes AM, Schlegelmilch T, Cohuet A, Awono-Ambene P, De Iorio M, Fontenille D, Morlais I, Christophides GK, Kafatos FC, Vlachou D: Conserved mosquito-parasite interactions affect development of Plasmodium falciparum in Africa. PLoS Pathog. 2008, 4: e1000069-10.1371/journal.ppat.1000069.PubMedCentralCrossRefPubMed
31.
Andreadis TG: Microsporidian parasites of mosquitoes. J Am Mosq Control Assoc. 2007, 23: 3-29. 10.2987/8756-971X(2007)23[3:MPOM]2.0.CO;2.CrossRefPubMed
32.
33.
Franke-Fayard B, Trueman H, Ramesar J, Mendoza J, van der Keur M, van der Linden R, Sinden RE, Waters AP, Janse CJ: A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol. 2004, 137: 23-33. 10.1016/j.molbiopara.2004.04.007.CrossRefPubMed
34.
Janse CJ, Franke-Fayard B, Mair GR, Ramesar J, Thiel C, Engelmann S, Matuschewski K, van Gemert GJ, Sauerwein RW, Waters AP: High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol. 2006, 145: 60-70. 10.1016/j.molbiopara.2005.09.007.CrossRefPubMed
35.
Akaike H: Information theory as an extension of the maximum likelihood principle. Second international symposium on information theory. Edited by: Petrov BN, Csaki F. 1973, Budapest, Hungary: Akademiai Kiado, 267-281.
36.
SAS Institute Inc: JMP 8. Cary, NC. 1989-2008.
37.
38.
39.
Fox CW, Czesak ME: Evolutionary ecology of progeny size in arthropods. Ann Rev Entomol. 2000, 45: 341-369. 10.1146/annurev.ento.45.1.341.CrossRef
40.
Gliwicz ZM, Guisande C: Family-planning in Daphnia: Resistance to starvation in offspring born to mothers grown at different food levels. Oecologia. 1992, 91: 463-467. 10.1007/BF00650317.CrossRef
41.
Mousseau TA, Fox CW: Maternal effects as adaptations. 1998, Oxford: Oxford University Press
42.
Huang CC, Song YL: Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Dev Comp Immunol. 1999, 23: 545-552. 10.1016/S0145-305X(99)00038-5.CrossRefPubMed
43.
Little TJ, O'Connor B, Colegrave N, Watt K, Read AF: Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol. 2003, 13: 489-492. 10.1016/S0960-9822(03)00163-5.CrossRefPubMed
44.
Sadd BM, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P: Trans-generational immune priming in a social insect. Biol Letters. 2005, 1: 386-388. 10.1098/rsbl.2005.0369.CrossRef
45.
Sadd BM, Schmid-Hempel P: Facultative but persistent transgenerational immunity via the mother's eggs in bumblebees. Curr Biol. 2007, 17: R1046-R1047. 10.1016/j.cub.2007.11.007.CrossRefPubMed
46.
Moret Y: 'Trans-generational immune priming': specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc R Soc London, B. 2006, 273: 1399-1405. 10.1098/rspb.2006.3465.CrossRef
47.
Zanchi C, Troussard JP, Martinaud G, Moreau J, Moret Y: Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. J Anim Ecol. 2011, 80: 1174-1183. 10.1111/j.1365-2656.2011.01872.x.CrossRefPubMed
48.
Dimopoulos G, Richman A, Muller HM, Kafatos FC: Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci USA. 1997, 94: 11508-11513. 10.1073/pnas.94.21.11508.PubMedCentralCrossRefPubMed
49.
Richman AM, Dimopoulos G, Seeley D, Kafatos FC: Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. EMBO J. 1997, 16: 6114-6119. 10.1093/emboj/16.20.6114.PubMedCentralCrossRefPubMed
50.
Lowenberger CA, Kamal S, Chiles J, Paskewitz S, Bulet P, Hoffmann JA, Christensen BM: Mosquito-Plasmodium interactions in response to immune activation of the vector. Exp Parasitol. 1999, 91: 59-69. 10.1006/expr.1999.4350.CrossRefPubMed
51.
Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, Kafatos FC: Genome expression analysis of Anopheles gambiae: Responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA. 2002, 99: 8814-8819. 10.1073/pnas.092274999.PubMedCentralCrossRefPubMed
52.
Dong YM, Aguilar R, Xi ZY, Warr E, Mongin E, Dimopoulos G: Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006, 2: 513-525.CrossRef
53.
Dong Y, Manfredini F, Dimopoulos G: Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009, 5: e1000423-10.1371/journal.ppat.1000423.PubMedCentralCrossRefPubMed
54.
Dong YM, Dimopoulos G: Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem. 2009, 284: 9835-9844. 10.1074/jbc.M807084200.PubMedCentralCrossRefPubMed
55.
Meister S, Agianian B, Turlure F, Relogio A, Morlais I, Kafatos FC, Christophides GK: Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog. 2009, 5: e1000542-10.1371/journal.ppat.1000542.PubMedCentralCrossRefPubMed
56.
Fox RM, Weiser J: A microsporidian parasite of Anopheles gambiae in Liberia. J Parasitol. 1959, 45: 21-30. 10.2307/3274782.CrossRefPubMed
57.
Hulls RH: The adverse effects of a microsporidian on sporogony and infectivity of Plasmodium berghei. Trans R Soc Trop Med Hyg. 1971, 65: 421-422.CrossRefPubMed
58.
Gajanana A, Tewari SC, Reuben R, Rajagopalan PK: Partial suppression of malaria parasites in Aedes aegypti and Anopheles stephensi doubly infected with Nosema algerae and Plasmodium. Indian J Med Res. 1979, 70: 417-423.PubMed
59.
Margos G, Maier WA, Seitz HM: The effect of nosematosis on the development of Plasmodium falciparum in Anopheles stephensi. Parasitol Res. 1992, 78: 168-171. 10.1007/BF00931661.CrossRefPubMed
60.
Schenker W, Maier WA, Seitz HM: The effects of Nosema algerae on the development of Plasmodium yoelii nigeriensis in Anopheles stephensi. Parasitol Res. 1992, 78: 56-59. 10.1007/BF00936182.CrossRefPubMed
61.
Biron DG, Agnew P, Marche L, Renault L, Sidobre C, Michalakis Y: Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis. Int J Parasitol. 2005, 35: 1385-1397. 10.1016/j.ijpara.2005.05.015.CrossRefPubMed
62.
Boots M, Begon M: Trade-offs with resistance to a granulosis-virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct Ecol. 1993, 7: 528-534. 10.2307/2390128.CrossRef
63.
Koella JC, Boëte C: A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution. 2002, 56: 1074-1079.CrossRefPubMed
64.
Rantala MJ, Roff DA: An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct Ecol. 2005, 19: 323-330. 10.1111/j.1365-2435.2005.00979.x.CrossRef
65.
Mooney KA, Halitschke R, Kessler A, Agrawal AA: Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science. 2010, 327: 1642-1644. 10.1126/science.1184814.CrossRefPubMed
66.
Thomas MB, Read AF: Can fungal biopesticides control malaria?. Nat Rev Microbiol. 2007, 5: 377-383. 10.1038/nrmicro1638.CrossRefPubMed
67.
Koella JC, Lorenz L, Bargielowski I: Microsporidians as evolution-proof agents of malaria control?. Adv Parasitol. 2009, 68: 315-327.CrossRefPubMed
Metadata
Title
Maternal environment shapes the life history and susceptibility to malaria of Anopheles gambiae mosquitoes
Authors
Lena M Lorenz
Jacob C Koella
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2011
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-10-382

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