Independent effects on cellular and humoral immune responses underlie genotype-by-genotype interactions between Drosophila and parasitoids

Autoři: Alexandre B. Leitão aff001;  Xueni Bian aff001;  Jonathan P. Day aff001;  Simone Pitton aff001;  Eşref Demir aff001;  Francis M. Jiggins aff001
Působiště autorů: Department of Genetics, University of Cambridge, Cambridge, United Kingdom aff001;  Antalya Bilim University, Faculty of Engineering, Department of Material Science and Nanotechnology Engineering, Dosemealti, Antalya, Turkey aff002
Vyšlo v časopise: Independent effects on cellular and humoral immune responses underlie genotype-by-genotype interactions between Drosophila and parasitoids. PLoS Pathog 15(10): e32767. doi:10.1371/journal.ppat.1008084
Kategorie: Research Article
doi: 10.1371/journal.ppat.1008084


It is common to find abundant genetic variation in host resistance and parasite infectivity within populations, with the outcome of infection frequently depending on genotype-specific interactions. Underlying these effects are complex immune defenses that are under the control of both host and parasite genes. We have found extensive variation in Drosophila melanogaster’s immune response against the parasitoid wasp Leptopilina boulardi. Some aspects of the immune response, such as phenoloxidase activity, are predominantly affected by the host genotype. Some, such as upregulation of the complement-like protein Tep1, are controlled by the parasite genotype. Others, like the differentiation of immune cells called lamellocytes, depend on the specific combination of host and parasite genotypes. These observations illustrate how the outcome of infection depends on independent genetic effects on different aspects of host immunity. As parasite-killing results from the concerted action of different components of the immune response, these observations provide a physiological mechanism to generate phenomena like epistasis and genotype-interactions that underlie models of coevolution.

Klíčová slova:

Drosophila melanogaster – Hemocytes – Host-pathogen interactions – Immune response – Immune suppression – Larvae – Parasitic diseases – Parasitism


1. Lambrechts L, Fellous S, Koella JC. Coevolutionary interactions between host and parasite genotypes. Trends Parasitol. 2006;22: 12–16. doi: 10.1016/ 16310412

2. Boots M, White A, Best A, Bowers R. How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites. Evolution. 2014; doi: 10.1111/evo.12393 24593303

3. Jaenike J. An hypothesis to account for the maintenance of sex within populations. Evol Theory. 1978;

4. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol. 2007;25: 697–743. doi: 10.1146/annurev.immunol.25.022106.141615 17201680

5. Marylène P, Dominique C, Jean-Luc G. Insights into function and evolution of parasitoid wasp venoms. Curr Opin Insect Sci. 2014; doi: 10.1016/j.cois.2014.10.004

6. Bergelson J, Kreitman M, Stahl EA, Tian D. Evolutionary dynamics of plant R-genes. Science. 2001. doi: 10.1126/science.1061337 11423651

7. Carpenter JA, Hadfield JD, Bangham J, Jiggins FM. Specific interactions between host and parasite genotypes do not act as a constraint on the evolution of antiviral resistance in drosophila. Evolution. 2012;66. doi: 10.1111/j.1558-5646.2011.01501.x 22486692

8. Bangham J, Obbard DJ, Kim K-W, Haddrill PR, Jiggins FM. The age and evolution of an antiviral resistance mutation in Drosophila melanogaster. Proc R Soc B Biol Sci. 2007;274. doi: 10.1098/rspb.2007.0611 17550883

9. Fleuriet A. Polymorphism of the hereditary sigma virus in natural populations of Drosophila melanogaster. Genetics. 1980;

10. Bento G, Routtu J, Fields PD, Bourgeois Y, Du Pasquier L, Ebert D. The genetic basis of resistance and matching-allele interactions of a host-parasite system: The Daphnia magna-Pasteuria ramosa model. PLoS Genet. 2017; doi: 10.1371/journal.pgen.1006596 28222092

11. Luijckx P, Fienberg H, Duneau D, Ebert D. A matching-allele model explains host resistance to parasites. Curr Biol. 2013; doi: 10.1016/j.cub.2013.04.064 23707426

12. Goulder PJR, Walker BD. HIV and HLA Class I: An Evolving Relationship. Immunity. 2012. doi: 10.1016/j.immuni.2012.09.005 22999948

13. Barribeau SM, Sadd BM, du Plessis L, Schmid-Hempel P. Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proc Natl Acad Sci. 2014; doi: 10.1073/pnas.1318628111 24550506

14. Ebert D, Duneau D, Hall MD, Luijckx P, Andras JP, Du Pasquier L, et al. A Population Biology Perspective on the Stepwise Infection Process of the Bacterial Pathogen Pasteuria ramosa in Daphnia. Adv Parasitol. 2016; doi: 10.1016/bs.apar.2015.10.001 27015951

15. Hall MD, Bento G, Ebert D. The Evolutionary Consequences of Stepwise Infection Processes. Trends in Ecology and Evolution. 2017. doi: 10.1016/j.tree.2017.05.009 28648806

16. Hall MD, Routtu J, Ebert D. Dissecting the genetic architecture of a stepwise infection process. Mol Ecol. John Wiley & Sons, Ltd (10.1111); 2019;0. doi: 10.1111/mec.15166 31283079

17. Hall MD, Ebert D. Disentangling the influence of parasite genotype, host genotype and maternal environment on different stages of bacterial infection in Daphnia magna. Proc R Soc B Biol Sci. 2012;279: 3176–3183. doi: 10.1098/rspb.2012.0509 22593109

18. Nuismer SL, Dybdahl MF. Quantifying the coevolutionary potential of multistep immune defenses. Evolution. 2016; doi: 10.1111/evo.12863 26792644

19. Fleury F, Ris N, Allemand R, Fouillet P, Carton Y, Boulétreau M. Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. Genetica. 2004;120: 181–94. doi: 10.1023/b:gene.0000017640.78087.9e 15088657

20. Mcgonigle JE, Leitão AB, Ommeslag S, Smith S, Day P, Jiggins FM. Parallel and costly changes to cellular immunity underlie the evolution of parasitoid resistance in three Drosophila species. PLoS Pathog. 2017;13(10): 1–20.

21. Kraaijeveld AR, Godfray HC. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature. 1997;389: 278–280. doi: 10.1038/38483 9305840

22. Kraaijeveld AR, van Alphen JJM. Geographical variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evol Ecol. Springer; 1995;9: 10–17. doi: 10.1007/BF01237692

23. Kraaijeveld AR, Alphen JJM Van. Geographical variation in encapsulation ability of parasitoid-specific components. Evol Ecol. 1995;9: 10–17. doi: 10.1007/BF01237692

24. Dupas S, Carton Y, Poiriè M. Genetic dimension of the coevolution of virulence-resistance in Drosophila—parasitoid wasp relationships. Heredity (Edinb). 2003;90: 84–9. doi: 10.1038/sj.hdy.6800182 12522430

25. Honti V, Csordás G, Kurucz É, Márkus R, Andó I. The cell-mediated immunity of Drosophila melanogaster: hemocyte lineages, immune compartments, microanatomy and regulation. Dev Comp Immunol. 2014;42: 47–56. doi: 10.1016/j.dci.2013.06.005 23800719

26. Carton Y, Poirié M, Nappi AJ. Insect immune resistance to parasitoids. Insect Sci. 2008;15: 67–87. doi: 10.1111/j.1744-7917.2008.00188.x

27. Labrosse C, Eslin P, Doury G, Drezen JM, Poirié M. Haemocyte changes in D. Melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor. J Insect Physiol. 2005;51: 161–70. doi: 10.1016/j.jinsphys.2004.10.004 15749101

28. Russo J, Brehélin M, Carton Y. Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. J Insect Physiol. 2001;47: 167–172. doi: 10.1016/s0022-1910(00)00102-5 11064023

29. Colinet D, Dubuffet A, Cazes D, Moreau S, Drezen J-M, Poirié M. A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Dev Comp Immunol. 2009;33: 681–9. doi: 10.1016/j.dci.2008.11.013 19109990

30. Dupas S, Frey F, Carton Y. A Single Parasitoid Segregating Factor Controls Immune Suppression in Drosophila. J Hered. 1998;89: 306–311. doi: 10.1093/jhered/89.4.306 9703687

31. Huang W, Massouras A, Inoue Y, Peiffer J, Ràmia M, Tarone AM, et al. Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res. 2014; doi: 10.1101/gr.171546.113 24714809

32. Schlenke TA, Morales J, Govind S, Clark AG. Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog. 2007;3: 1486–1501. doi: 10.1371/journal.ppat.0030158 17967061

33. Dostálová A, Rommelaere S, Poidevin M, Lemaitre B. Thioester-containing proteins regulate the Toll pathway and play a role in Drosophila defence against microbial pathogens and parasitoid wasps. BMC Biol. BMC Biology; 2017; 1–16. doi: 10.1186/s12915-016-0343-5

34. Poirié M, Colinet D, Gatti JL. Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science. 2014. doi: 10.1016/j.cois.2014.10.004

35. Colinet D, Deleury E, Anselme C, Cazes D, Poulain J, Azema-Dossat C, et al. Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: The case of Leptopilina parasitoids of Drosophila. Insect Biochem Mol Biol. 2013; doi: 10.1016/j.ibmb.2013.03.010 23557852

36. Colinet D, Schmitz A, Cazes D, Gatti JL, Poirié M. The origin of intraspecific variation of virulence in an eukaryotic immune suppressive parasite. PLoS Pathog. 2010; doi: 10.1371/journal.ppat.1001206 21124871

37. Blandin SA, Wang-Sattler R, Lamacchia M, Gagneur J, Lycett G, Ning Y, et al. Dissecting the Genetic Basis of Resistance to Malaria Parasites in Anopheles gambiae. Science. 2009;326: 147–150. doi: 10.1126/science.1175241 19797663

38. Little TJ, Hultmark D, Read AF. Invertebrate immunity and the limits of mechanistic immunology. Nat Immunol. 2005;6: 651–4. doi: 10.1038/ni1219 15970937

39. Schmid-Hempel P. Parasite immune evasion: a momentous molecular war. Trends in Ecology and Evolution. 2008. doi: 10.1016/j.tree.2008.02.011 18439709

40. Kraaijeveld AR, Limentani EC, Godfray HC. Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc Biol Sci. 2001;268: 259–61. doi: 10.1098/rspb.2000.1354 11217895

41. Peters AD, Lively CM. The Red Queen and Fluctuating Epistasis: A Population Genetic Analysis of Antagonistic Coevolution. Am Nat. 1999;154: 393–405. doi: 10.1086/303247 10523486

42. Varaldi J, Petit S, Boulétreau M, Fleury F. The virus infecting the parasitoid Leptopilina boulardi exerts a specific action on superparasitism behaviour. Parasitology. 2006;132: 747–756. doi: 10.1017/S0031182006009930 16700960

43. Longdon B, Hadfield JD, Day JP, Smith SCL, McGonigle JE, Cogni R, et al. The Causes and Consequences of Changes in Virulence following Pathogen Host Shifts. PLoS Pathog. 2015;11: 1–18. doi: 10.1371/journal.ppat.1004728 25774803

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PLOS Pathogens

2019 Číslo 10

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