Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-12-05T11:40:40.547Z Has data issue: false hasContentIssue false

Can Wolbachia modulate the fecundity costs of Plasmodium in mosquitoes?

Published online by Cambridge University Press:  08 August 2017

F Zélé*
Affiliation:
cE3c: centre for Ecology, Evolution and Environmental changes, Faculdade de Ciencias, Universidade de Lisboa, Edificio C2, 3° Piso Campo Grande, 1749016 Lisbon, Portugal
O Duron
Affiliation:
Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle, CNRS (UMR 5290), Centre de Recherche IRD, 911 Avenue Agropolis, 34394 Montpellier, France Institut des Sciences de l'Evolution, CNRS (UMR 5554), University of Montpellier, 34090 Montpellier, France
A Rivero
Affiliation:
Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle, CNRS (UMR 5290), Centre de Recherche IRD, 911 Avenue Agropolis, 34394 Montpellier, France
*
Author for correspondence: F. Zélé, E-mail: fezele@fc.ul.pt

Abstract

Vertically transmitted parasites (VTPs) such as Wolbachia are expected not only to minimize the damage they inflict on their hosts, but also to protect their hosts against the damaging effects of coinfecting parasites. By modifying the fitness costs of the infection, VTPs can therefore play an important role in the evolution and epidemiology of infectious diseases.

Using a natural system, we explore the effects of a Wolbachia–Plasmodium co-infection on mosquito fecundity. While Plasmodium is known to frequently express its virulence by partially castrating its mosquito vectors, the effects of Wolbachia infections on mosquito fecundity are, in contrast, highly variable. Here, we show that Plasmodium drastically decreases the fecundity of mosquitoes by ca. 20%, and we provide the first evidence that this decrease is independent of the parasite's burden. Wolbachia, on the other hand, increases fecundity by roughly 10%, but does not alter the tolerance (fecundity–burden relationship) of mosquitoes to Plasmodium infection.

Although Wolbachia-infected mosquitoes fare overall better than uninfected ones, Wolbachia does not confer a sufficiently high reproductive boost to mosquitoes to compensate for the reproductive losses inflicted by Plasmodium. We discuss the potential mechanisms and implications underlying the conflicting effects of these two parasites on mosquito reproduction.

Type
Research Article
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.)

Footnotes

Co-last authors.

References

Ahmed, AM, et al. (2001) Effects of malaria infection on vitellogenesis in Anopheles gambiae during two gonotrophic cycles. Insect Molecular Biology 10, 347356.CrossRefGoogle ScholarPubMed
Armbruster, P and Hutchinson, RA (2002) Pupal mass and wing length as indicators of fecundity in Aedes albopictus and Aedes geniculatus (Diptera : culicidae). Journal of Medical Entomology 39, 699704.CrossRefGoogle ScholarPubMed
Atyame, CM, et al. (2011) Diversification of Wolbachia endosymbiont in the Culex pipiens mosquito. Molecular Biology and Evolution 28, 27612772.CrossRefGoogle ScholarPubMed
Balmer, O, et al. (2009) Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90, 33673378.CrossRefGoogle ScholarPubMed
Baton, LA, et al. (2013) wFlu: characterization and evaluation of a native Wolbachia from the mosquito Aedes fluviatilis as a potential vector control agent. PLoS ONE 8, e59619.CrossRefGoogle ScholarPubMed
Bazzocchi, C, et al. (2007) Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunology 29, 7379.CrossRefGoogle ScholarPubMed
Ben-Ami, F, Rigaud, T and Ebert, D (2011) The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies. Journal of Evolutionary Biology 24, 13071316.CrossRefGoogle ScholarPubMed
Bensch, S, Hellgren, O and Perez-Tris, J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 13531358.CrossRefGoogle ScholarPubMed
Bolker, BM (2008) Ecological Models and Data in R. Princeton University Press, New Jersey.Google Scholar
Briegel, H (1990) Metabolic relationship between female body size, reserves and fecundity of Aedes aegypti. Journal of Insect Physiology 36, 165172.CrossRefGoogle Scholar
Brownlie, JC, et al. (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathogens 5, e1000368.CrossRefGoogle ScholarPubMed
Bull, JJ, Molineux, IJ and Rice, WR (1991) Selection of benevolence in a host-parasite system. Evolution 45, 875882.Google Scholar
Caragata, EP, et al. (2016) Diet-Induced nutritional stress and pathogen interference in Wolbachia-infected Aedes aegypti. PLoS Neglected Tropical Diseases 10, e0005158.CrossRefGoogle ScholarPubMed
Carwardine, SL and Hurd, H (1997) Effects of Plasmodium yoelii nigeriensis infection on Anopheles stephensi egg development and resorption. Medical and Veterinary Entomology 11, 265269.CrossRefGoogle ScholarPubMed
Churcher, TS, et al. (2017) Probability of transmission of malaria from mosquito to human is regulated by mosquito parasite density in naïve and vaccinated hosts. PLoS Pathogens 13, e1006108.CrossRefGoogle Scholar
Crawley, MJ (2007) The R Book. John Wiley & Sons, Ltd, Chichester, England.CrossRefGoogle Scholar
Dawes, EJ, et al. (2009) Anopheles mortality is both age- and Plasmodium-density dependent: implications for malaria transmission. Malaria Journal 8, 228. doi: 10.1186/1475-2875-8-228.CrossRefGoogle ScholarPubMed
Dobson, SL, Marsland, EJ and Rattanadechakul, W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160, 10871094.CrossRefGoogle ScholarPubMed
Dumas, E, et al. (2013) Population structure of Wolbachia and cytoplasmic introgression in a complex of mosquito species. BMC Evolutionary Biology 13, 181. doi: 10.1186/1471-2148-13-181.CrossRefGoogle Scholar
Duron, O, et al. (2005) Transposable element polymorphism of Wolbachia in the mosquito Culex pipiens: evidence of genetic diversity, superinfection and recombination. Molecular Ecology 14, 15611573.CrossRefGoogle ScholarPubMed
Duron, O, Fort, P and Weill, M (2006 a). Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens. Proceedings of the Royal Society of London Series B: Biological Sciences 273, 495502.Google ScholarPubMed
Duron, O, et al. (2006 b). High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoes. Evolution 60, 303314.Google ScholarPubMed
Ebert, D and Herre, EA (1996) The evolution of parasitic diseases. Parasitology Today 12, 96101.CrossRefGoogle ScholarPubMed
Engelstadter, J and Hurst, GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology Evolution and Systematics 40, 127149.CrossRefGoogle Scholar
Fast, EM, et al. (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334, 990992.CrossRefGoogle ScholarPubMed
Ferguson, HM, Rivero, A and Read, AF (2003) The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitology 127, 919.CrossRefGoogle ScholarPubMed
Fournier, DA, et al. (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods and Software 27, 233249.CrossRefGoogle Scholar
Fu, Y, et al. (2010) Artificial triple Wolbachia infection in Aedes albopictus yields a new pattern of unidirectional cytoplasmic incompatibility. Applied and Environmental Microbiology 76, 58875891. doi: 10.1128/aem.00218-10.CrossRefGoogle ScholarPubMed
Georghiou, GP, Metcalf, RL and Gidden, FE (1966) Carbamate-resistance in mosquitos – selection of Culex pipiens fatigans wiedemann (=C. quinquefasciatus say) for resistance to baygon. Bulletin of the World Health Organization 35, 691708.Google Scholar
Haine, ER (2008) Symbiont-mediated protection. Proceedings of the Royal Society B-Biological Sciences 275, 353361.CrossRefGoogle ScholarPubMed
Haine, ER, Boucansaud, K and Rigaud, T (2005) Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society of London Series B: Biological Sciences 272, 25052510.Google ScholarPubMed
Hoffmann, AA, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476, 454457.CrossRefGoogle ScholarPubMed
Hoffmann, AA, Ross, PA and Rasic, G (2015) Wolbachia strains for disease control: ecological and evolutionary considerations. Evolutionary Applications 8, 751768.CrossRefGoogle ScholarPubMed
Hogg, JC and Hurd, H (1995) Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size ofAnopheles stephensi during three gonotrophic cycles. Parasitology 111, 555562.CrossRefGoogle Scholar
Hogg, JC, Carwardine, S and Hurd, H (1997) The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Parasitology Research 83, 374379.CrossRefGoogle ScholarPubMed
Hopwood, JA, et al. (2001) Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. Journal of Experimental Biology 204, 27732780.CrossRefGoogle ScholarPubMed
Hurd, H (2003) Manipulation of medically important insect vectors by their parasites. Annual Review of Entomology 48, 141161.CrossRefGoogle ScholarPubMed
Hurd, H (2009) Evolutionary drivers of parasite-induced changes in insect life-history traits: from theory to underlying mechanisms. Advances in Parasitology 68, 85110.CrossRefGoogle Scholar
Jaenike, J (1996) Suboptimal virulence of an insect-parasitic nematode. Evolution 50, 22412247.Google ScholarPubMed
Jiggins, FM and Hurst, GDD (2011) Rapid insect evolution by symbiont transfer. Science 332, 185186.CrossRefGoogle ScholarPubMed
Jones, EO, White, A and Boots, M (2010) The evolutionary implications of conflict between parasites with different transmission modes. Evolution 64, 24082416.Google ScholarPubMed
Joshi, D, et al. (2014) Wolbachia strain wAlbB confers both fitness costs and benefit on Anopheles stephensi. Parasites & Vectors 7. doi: 10.1186/1756-3305-7-336.CrossRefGoogle ScholarPubMed
Kremer, N, et al. (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathogens 5, e1000630.CrossRefGoogle ScholarPubMed
Lipsitch, M, Siller, S and Nowak, MA (1996) The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 17201741.CrossRefGoogle ScholarPubMed
McMeniman, CJ, et al. (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323, 141144.CrossRefGoogle ScholarPubMed
Mideo, N (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268.CrossRefGoogle ScholarPubMed
Morand, S (2011) The impact of multiple infections on wild animal hosts: a review. Infection Ecology & Epidemiology 1, 7346. doi: 10.3402/iee.v1i0.7346.Google Scholar
Murdock, CC, et al. (2014) Temperature alters Plasmodium blocking by Wolbachia. Scientific Reports 4, 3932.CrossRefGoogle ScholarPubMed
Nguyen, TH, et al. (2015) Field evaluation of the establishment potential of wMelPop Wolbachia in Australia and Vietnam for dengue control. Parasites & Vectors 8, 563. doi: 10.1186/s13071-015-1174-x.CrossRefGoogle ScholarPubMed
O'Keefe, KJ and Antonovics, J (2002) Playing by different rules: the evolution of virulence in sterilizing pathogens. American Naturalist 159, 597605.CrossRefGoogle ScholarPubMed
Pannebakker, BA, et al. (2007) Parasitic inhibition of cell death facilitates symbiosis. Proceedings of the National Academy of Sciences of the United States of America 104, 213215.CrossRefGoogle ScholarPubMed
Pigeault, R, et al. (2015) Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology of Plasmodium. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 370, 20140300. doi: 10.1098/rstb.2014.0300.Google Scholar
Raberg, L, Sim, D and Read, AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812814.CrossRefGoogle ScholarPubMed
Rasgon, JL and Scott, TW (2003) Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics 165, 20292038.CrossRefGoogle ScholarPubMed
Read, AF, Graham, AL and Raberg, L (2008) Animal defenses against infectious agents: is damage control more important than pathogen control? PLoS Biology 6, 26382641.CrossRefGoogle ScholarPubMed
Rodrigues, LR, et al. (2016) Integrating competition for food, hosts, or mates via experimental evolution. Trends in Ecology & Evolution 31, 158170.CrossRefGoogle ScholarPubMed
Schwartz, A and Koella, JC (2001) Trade-offs, conflicts of interest and manipulation in Plasmodium-mosquito interactions. Trends in Parasitology 17, 189194.CrossRefGoogle ScholarPubMed
Service, MW (1993) Mosquito Ecology: Field Sampling Methods, 2nd Edn. Elsevier Applied Science, London.Google Scholar
Shaw, WR, et al. (2016) Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development. Nature Communications 7, 11772. doi: 10.1038/ncomms11772.CrossRefGoogle ScholarPubMed
Smith, JE and Dunn, AM (1991) Transovarial transmission. Parasitology Today 7, 146148.CrossRefGoogle ScholarPubMed
Sternberg, ED, et al. (2012) Food plant derived disease tolerance and resistance in natural buterfly-plant-parasite interactions. Evolution 66, 33673376.CrossRefGoogle ScholarPubMed
Turelli, M (1994) Evolution of incompatibility-inducing microbes and their hosts. Evolution 48, 15001513.Google ScholarPubMed
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, Florida.Google Scholar
Vézilier, J, et al. (2010) Insecticide resistance and malaria transmission: infection rate and oocyst burden in Culex pipiens mosquitoes infected with Plasmodium relictum. Malaria Journal 9, 379.CrossRefGoogle ScholarPubMed
Vézilier, J, et al. (2012) Plasmodium infection decreases fecundity and increases survival of mosquitoes. Proceedings of the Royal Society of London Series B: Biological Sciences 279, 40334041.Google ScholarPubMed
Waldenstrom, J, et al. (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191194.CrossRefGoogle ScholarPubMed
Walker, T, et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476, 450453.CrossRefGoogle ScholarPubMed
Werren, JH, Baldo, L and Clark, ME (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741751.CrossRefGoogle ScholarPubMed
Xi, ZY, Khoo, CCH and Dobson, SL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310, 326328.CrossRefGoogle Scholar
Zélé, F, et al. (2012) Infection with Wolbachia protects mosquitoes against Plasmodium-induced mortality in a natural system. Journal of Evolutionary Biology 25, 12431252.CrossRefGoogle Scholar
Zélé, F, et al. (2014 a). Wolbachia increases susceptibility to Plasmodium infection in a natural system. Proceedings of the Royal Society of London Series B: Biological Sciences 281, 20132837.Google Scholar
Zélé, F, et al. (2014 b). Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance. Parasites & Vectors 7, 437.CrossRefGoogle ScholarPubMed
Zug, R and Hammerstein, P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews 90, 89111.CrossRefGoogle Scholar
Supplementary material: PDF

Zele supplementary material

Tables S1-S2 and Figures S1-S3

Download Zele supplementary material(PDF)
PDF 633 KB