Does membrane feeding compromise the quality of Aedes aegypti mosquitoes?

Autoři: Perran A. Ross aff001;  Meng-Jia Lau aff001;  Ary A. Hoffmann aff001
Působiště autorů: Pest and Environmental Adaptation Research Group, Bio21 Institute and the School of BioSciences, The University of Melbourne, Parkville, Victoria, Australia aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224268


Modified Aedes aegypti mosquitoes are being mass-reared for release in disease control programs around the world. Releases involving female mosquitoes rely on them being able to seek and feed on human hosts. To facilitate the mass-production of mosquitoes for releases, females are often provided blood through artificial membrane feeders. When reared across generations there is a risk that mosquitoes will adapt to feeding on membranes and lose their ability to feed on human hosts. To test adaptation to membrane feeding, we selected replicate populations of Ae. aegypti for feeding on either human arms or membrane feeders for at least 8 generations. Membrane-selected populations suffered fitness costs, likely due to inbreeding depression arising from bottlenecks. Membrane-selected females had higher feeding rates on membranes than human-selected ones, suggesting adaptation to membrane feeding, but they maintained their attraction to host cues and feeding ability on humans despite a lack of selection for these traits. Host-seeking ability in small laboratory cages did not differ between populations selected on the two blood sources, but membrane-selected females were compromised in a semi-field enclosure where host-seeking was tested over a longer distance. Our findings suggest that Ae. aegypti may adapt to feeding on blood provided artificially, but this will not substantially compromise field performance or affect experimental assessments of mosquito fitness. However, large population sizes (thousands of individuals) during mass rearing with membrane feeders should be maintained to avoid bottlenecks which lead to inbreeding depression.

Klíčová slova:

Aedes aegypti – Artificial membranes – Blood – Fecundity – Inbreeding – Membrane potential – Mosquitoes


1. Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, et al. Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis. 2017;11(7):e0005625. doi: 10.1371/journal.pntd.0005625 28727779

2. Benedict M, Robinson AS. The first releases of transgenic mosquitoes: an argument for the sterile insect technique. Trends Parasitol. 2003;19(8):349–55. doi: 10.1016/s1471-4922(03)00144-2 12901936

3. Carvalho DO, McKemey AR, Garziera L, Lacroix R, Donnelly CA, Alphey L, et al. Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes. PLoS Negl Trop Dis. 2015;9(7):e0003864. doi: 10.1371/journal.pntd.0003864 26135160

4. Mains JW, Kelly PH, Dobson KL, Petrie WD, Dobson SL. Localized control of Aedes aegypti (Diptera: Culicidae) in Miami, FL, via inundative releases of Wolbachia-infected male mosquitoes. J Med Entomol. 2019.

5. Ross PA, Turelli M, Hoffmann AA. Evolutionary ecology of Wolbachia releases for disease control. Annu Rev Genet. 2019;53(1). doi: 10.1146/annurev-genet-112618-043609 31505135

6. Gantz VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM, Bier E, et al. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci USA. 2015;112(49):E6736–E43. doi: 10.1073/pnas.1521077112 26598698

7. Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C, Katsanos D, et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nature Biotechnol. 2016;34(1):78–83. doi: 10.1038/nbt.3439 26641531

8. Kyrou K, Hammond AM, Galizi R, Kranjc N, Burt A, Beaghton AK, et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nature Biotechnol. 2018;36(11):1062–6. doi: 10.1038/nbt.4245 30247490

9. Helinski ME, Harrington LC. Considerations for male fitness in successful genetic vector control programs. Ecology of parasite-vector interactions: Springer; 2013. p. 221–44.

10. Carvalho DO, Nimmo D, Naish N, McKemey AR, Gray P, Wilke AB, et al. Mass production of genetically modified Aedes aegypti for field releases in Brazil. J Vis Exp. 2014;(83):e3579. doi: 10.3791/3579 24430003

11. Hoffmann AA, Ross PA. Rates and patterns of laboratory adaptation in (mostly) insects. J Econ Entomol. 2018;111(2):501–9. doi: 10.1093/jee/toy024 29506036

12. Clark GG, Bernier UR, Allan SA, Kline DL, Golden FV. Changes in host-seeking behavior of Puerto Rican Aedes aegypti after colonization. J Med Entomol. 2011;48(3):533–7. doi: 10.1603/me10207 21661313

13. Grossman MK, Uc-Puc V, Rodriguez J, Cutler DJ, Morran LT, Manrique-Saide P, et al. Restoration of pyrethroid susceptibility in a highly resistant Aedes aegypti population. Biol Lett. 2018;14(6). doi: 10.1098/rsbl.2018.0022 29899128

14. Ross PA, Endersby-Harshman NM, Hoffmann AA. A comprehensive assessment of inbreeding and laboratory adaptation in Aedes aegypti mosquitoes. Evol Appl. 2019;12(3):572–86. doi: 10.1111/eva.12740 30828375

15. Briegel H, Hefti M, DiMarco E. Lipid metabolism during sequential gonotrophic cycles in large and small female Aedes aegypti. J Insect Physiol. 2002;48(5):547–54. doi: 10.1016/s0022-1910(02)00072-0 12770082

16. Ross PA, Axford JK, Richardson KM, Endersby-Harshman NM, Hoffmann AA. Maintaining Aedes aegypti mosquitoes infected with Wolbachia. J Vis Exp. 2017;(126). doi: 10.3791/56124 28829414

17. Scott TW, Chow E, Strickman D, Kittayapong P, Wirtz RA, Lorenz LH, et al. Blood-feeding patterns of Aedes aegypti (Diptera: Culicidae) collected in a rural Thai village. J Med Entomol. 1993;30(5):922–7. doi: 10.1093/jmedent/30.5.922 8254642

18. Harrington LC, Edman JD, Scott TW. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol. 2001;38(3):411–22. doi: 10.1603/0022-2585-38.3.411 11372967

19. McMeniman CJ, Hughes GL, O’Neill SL. A Wolbachia symbiont in Aedes aegypti disrupts mosquito egg development to a greater extent when mosquitoes feed on nonhuman versus human blood. J Med Entomol. 2011;48(1):76–84. doi: 10.1603/me09188 21337952

20. Caragata EP, Rances E, O’Neill SL, McGraw EA. Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol. 2014;67(1):205–18. doi: 10.1007/s00248-013-0339-4 24337107

21. Paris V, Cottingham E, Ross PA, Axford JK, Hoffmann AA. Effects of alternative blood sources on Wolbachia infected Aedes aegypti females within and across generations. Insects. 2018;9(4). doi: 10.3390/insects9040140 30314399

22. Gonzales KK, Rodriguez SD, Chung HN, Kowalski M, Vulcan J, Moore EL, et al. The effect of SkitoSnack, an artificial blood meal replacement, on Aedes aegypti life history traits and gut microbiota. Sci Rep. 2018;8(1):11023. doi: 10.1038/s41598-018-29415-5 30038361

23. Dutra HLC, Rodrigues SL, Mansur SB, de Oliveira SP, Caragata EP, Moreira LA. Development and physiological effects of an artificial diet for Wolbachia-infected Aedes aegypti. Sci Rep. 2017;7(1):15687. doi: 10.1038/s41598-017-16045-6 29146940

24. Baughman T, Peterson C, Ortega C, Preston SR, Paton C, Williams J, et al. A highly stable blood meal alternative for rearing Aedes and Anopheles mosquitoes. PLoS Negl Trop Dis. 2017;11(12):e0006142. doi: 10.1371/journal.pntd.0006142 29287072

25. Marques J, Cardoso JCR, Felix RC, Santana RAG, Guerra MdGB, Power D, et al. Fresh-blood-free diet for rearing malaria mosquito vectors. Sci Rep. 2018;8(1):17807. doi: 10.1038/s41598-018-35886-3 30546023

26. Gonzales KK, Hansen IA. Artificial diets for mosquitoes. Int J Environ Res Public Health. 2016;13(12). doi: 10.3390/ijerph13121267 28009851

27. Romano D, Stefanini C, Canale A, Benelli G. Artificial blood feeders for mosquitoes and ticks—Where from, where to? Acta Trop. 2018;183:43–56. doi: 10.1016/j.actatropica.2018.04.009 29625092

28. Dias LDS, Bauzer L, Lima JBP. Artificial blood feeding for Culicidae colony maintenance in laboratories: does the blood source condition matter? Rev Inst Med Trop Sao Paulo. 2018;60:e45. doi: 10.1590/s1678-9946201860045 30231167

29. Costa-da-Silva AL, Navarrete FR, Salvador FS, Karina-Costa M, Ioshino RS, Azevedo DS, et al. Glytube: A conical tube and Parafilm M-based method as a simplified device to artificially blood-feed the dengue vector mosquito, Aedes aegypti. PloS One. 2013;8(1):e53816. doi: 10.1371/journal.pone.0053816 23342010

30. Luo Y-P. A novel multiple membrane blood-feeding system for investigating and maintaining Aedes aegypti and Aedes albopictus mosquitoes. J Vector Ecol. 2014;39(2):271–7. doi: 10.1111/jvec.12101 25424255

31. Phasomkusolsil S, Tawong J, Monkanna N, Pantuwatana K, Damdangdee N, Khongtak W, et al. Maintenance of mosquito vectors: effects of blood source on feeding, survival, fecundity, and egg hatching rates. J Vector Ecol. 2013;38(1):38–45. doi: 10.1111/j.1948-7134.2013.12006.x 23701605

32. Deng L, Koou S-Y, Png AB, Ng LC, Lam-Phua SG. A novel mosquito feeding system for routine blood-feeding of Aedes aegypti and Aedes albopictus. Trop Biomed. 2012;29(1):169–74. 22543617

33. Siria DJ, Batista EP, Opiyo MA, Melo EF, Sumaye RD, Ngowo HS, et al. Evaluation of a simple polytetrafluoroethylene (PTFE)-based membrane for blood-feeding of malaria and dengue fever vectors in the laboratory. Parasit Vectors. 2018;11(1):236. doi: 10.1186/s13071-018-2823-7 29642937

34. Rutledge L, Ward R, Gould D. Studies on the feeding response of mosquitoes to nutritive solutions in a new membrane feeder. Mosq News. 1964;24(4):407–9.

35. Novak MG, Berry WJ, Rowley WA. Comparison of four membranes for artificially bloodfeeding mosquitoes. J Am Mosq Control Assoc. 1991;7(2):327–9. 1680153

36. Gunathilaka N, Ranathunge T, Udayanga L, Abeyewickreme W. Efficacy of blood sources and artificial blood feeding methods in rearing of Aedes aegypti (Diptera: Culicidae) for sterile insect technique and incompatible insect technique approaches in Sri Lanka. BioMed Res Int. 2017;2017:7. doi: 10.1155/2017/3196924 28894749

37. van Breugel F, Riffell J, Fairhall A, Dickinson MH. Mosquitoes use vision to associate odor plumes with thermal targets. Curr Biol. 2015;25(16):2123–9. doi: 10.1016/j.cub.2015.06.046 26190071

38. McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell. 2014;156(5):1060–71. doi: 10.1016/j.cell.2013.12.044 24581501

39. Vinauger C, Van Breugel F, Locke L, Tobin K, Dickinson M, Fairhall A, et al. Visual-olfactory integration in the human disease vector mosquito, Aedes aegypti. Curr Biol. 2019;29:1–8.

40. Liu MZ, Vosshall LB. General visual and contingent thermal cues interact to elicit attraction in female Aedes aegypti mosquitoes. Curr Biol. 2019;29(13):2250–7. doi: 10.1016/j.cub.2019.06.001 31257144

41. Choumet V, Attout T, Chartier L, Khun H, Sautereau J, Robbe-Vincent A, et al. Visualizing non infectious and infectious Anopheles gambiae blood feedings in naive and saliva-immunized mice. PloS One. 2012;7(12):e50464. doi: 10.1371/journal.pone.0050464 23272060

42. Rueda LM. Pictorial keys for the identification of mosquitoes (Diptera: Culicidae) associated with dengue virus transmission. Zootaxa. 2004;589(1):1–60.

43. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature. 2011;476(7361):454–7. doi: 10.1038/nature10356 21866160

44. Ross PA, Endersby NM, Hoffmann AA. Costs of three Wolbachia infections on the survival of Aedes aegypti larvae under starvation conditions. PLoS Negl Trop Dis. 2016;10(1):e0004320. doi: 10.1371/journal.pntd.0004320 26745630

45. Lau M-J, Endersby-Harshman NM, Axford JK, Ritchie SA, Hoffmann AA, Ross PA. Measuring the host-seeking ability of Aedes aegypti destined for field release. bioRxiv. 2019:695528. doi: 10.1101/695528

46. Ritchie SA, Johnson PH, Freeman AJ, Odell RG, Graham N, DeJong PA, et al. A secure semi-field system for the study of Aedes aegypti. PLoS Negl Trop Dis. 2011;5(3):e988. doi: 10.1371/journal.pntd.0000988 21445333

47. DeGennaro M, McBride CS, Seeholzer L, Nakagawa T, Dennis EJ, Goldman C, et al. orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET. Nature. 2013;498(7455):487–91. doi: 10.1038/nature12206 23719379

48. Garcia GdA, Sylvestre G, Aguiar R, da Costa GB, Martins AJ, Lima JBP, et al. Matching the genetics of released and local Aedes aegypti populations is critical to assure Wolbachia invasion. PLoS Negl Trop Dis. 2019;13(1):e0007023. doi: 10.1371/journal.pntd.0007023 30620733

49. Chadee DD, Beier JC. Factors influencing the duration of blood-feeding by laboratory-reared and wild Aedes aegypti (Diptera: Culicidae) from Trinidad, West Indies. Ann Trop Med Parasitol. 1997;91(2):199–207. doi: 10.1080/00034983.1997.11813130 9307662

50. Zhang D, Li Y, Sun Q, Zheng X, Gilles JRL, Yamada H, et al. Establishment of a medium-scale mosquito facility: tests on mass production cages for Aedes albopictus (Diptera: Culicidae). Parasit Vectors. 2018;11(1):189. doi: 10.1186/s13071-018-2750-7 29554945

51. Lacey ES, Ray A, Carde RT. Close encounters: contributions of carbon dioxide and human skin odour to finding and landing on a host in Aedes aegypti. Physiol Entomol. 2014;39(1):60–8. doi: 10.1111/phen.12048 24839345

52. Bidlingmayer W, Hem D. The range of visual attraction and the effect of competitive visual attractants upon mosquito (Diptera: Culicidae) flight. Bull Entomol Res. 1980;70(2):321–42.

53. Yeap HL, Mee P, Walker T, Weeks AR, O’Neill SL, Johnson P, et al. Dynamics of the “popcorn” Wolbachia infection in outbred Aedes aegypti informs prospects for mosquito vector control. Genetics. 2011;187(2):583–595. doi: 10.1534/genetics.110.122390 21135075

Článek vyšel v časopise


2019 Číslo 11