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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Evolution of host preference in anthropophilic mosquitoes

Authors: Chris Stone, Kevin Gross

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Insecticide-treated bed nets (ITNs) have played a large role in reducing the burden of malaria. There is concern however regarding the potential of the mass distributions and use of ITNs to select for insecticide and behavioural resistance in mosquito populations. A key feature of the vectorial capacity of the major sub-Saharan African malaria vector Anopheles gambiae sensu stricto (s.s.) is its tendency to feed almost exclusively on humans. Here, an evolutionary model is used to investigate the potential for ITNs to select for increased zoophily in this highly anthropophilic species and how this is influenced by ecological and operational conditions.

Results

The evolution of a single trait, namely the tendency to accept cattle as hosts, is modelled in mosquito populations which initially only bite humans. Thus, the conditions under which a resource specialist would broaden its diet and become a generalist are investigated. The results indicate that in the absence of insecticide-treated nets, host specialization in mosquitoes is either driven toward human specialization (when humans are more abundant than alternative hosts), or displays evolutionary bistability. The latter implies that the evolutionary endpoint relies on the initial trait value of the population. Bed nets select for increased zoophily while in use. When ITNs are removed, whether or not the population reverts to anthropophagic or zoophagic behaviour depends on whether the intervention had been maintained sufficiently long to drive the population past the evolutionarily unstable point.

Conclusions

The use of ITNs is likely to select for an increase in the biting preference for cattle. Bed nets may thus alter the population composition of major vector species in a manner that has positive epidemiological ramifications. Whether populations are set on a trajectory toward increased zoophily following the cessation of intense bed net usage in an area depends on the composition of host communities as well as operational conditions. This has potential implications for bed net campaigns, particularly with an eye toward scaling down interventions following interruption of transmission. Further research on malaria mosquito feeding behaviour is warranted to explore the conditions under which such adaptive shifts may actually occur in the field.
Literature
1.
go back to reference Futuyma DJ, Moreno G. The evolution of ecological specialization. Ann Rev Ecol Syst. 1988;19(1):207–33.CrossRef Futuyma DJ, Moreno G. The evolution of ecological specialization. Ann Rev Ecol Syst. 1988;19(1):207–33.CrossRef
2.
go back to reference Egas M, Dieckmann U, Sabelis MW. Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. Am Nat. 2004;163(4):518–31.CrossRefPubMed Egas M, Dieckmann U, Sabelis MW. Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. Am Nat. 2004;163(4):518–31.CrossRefPubMed
3.
go back to reference Ravigné V, Dieckmann U, Olivieri I. Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat. 2009;174(4):E141–69.CrossRefPubMed Ravigné V, Dieckmann U, Olivieri I. Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat. 2009;174(4):E141–69.CrossRefPubMed
4.
go back to reference Chubaty AM, Ma BO, Stein RW, Gillespie DR, Henry LM, Phelan C, et al. On the evolution of omnivory in a community context. Ecol Evol. 2014;4(3):251–65.CrossRefPubMed Chubaty AM, Ma BO, Stein RW, Gillespie DR, Henry LM, Phelan C, et al. On the evolution of omnivory in a community context. Ecol Evol. 2014;4(3):251–65.CrossRefPubMed
5.
go back to reference Jaenike J. Host specialization in phytophagous insects. Ann Rev Ecol Syst. 1990;21(1):243–73.CrossRef Jaenike J. Host specialization in phytophagous insects. Ann Rev Ecol Syst. 1990;21(1):243–73.CrossRef
6.
go back to reference Bernays E. The value of being a resource specialist: behavioral support for a neural hypothesis. Am Nat. 1998;151(5):451–64.CrossRefPubMed Bernays E. The value of being a resource specialist: behavioral support for a neural hypothesis. Am Nat. 1998;151(5):451–64.CrossRefPubMed
7.
go back to reference Bernays EA, Funk DJ. Specialists make faster decisions than generalists: experiments with aphids. Proc R Soc B. 1999;266(1415):151–6.CrossRef Bernays EA, Funk DJ. Specialists make faster decisions than generalists: experiments with aphids. Proc R Soc B. 1999;266(1415):151–6.CrossRef
8.
go back to reference Fry JD. The evolution of host specialization: are trade-offs overrated? Am Nat. 1996;148:S84–107.CrossRef Fry JD. The evolution of host specialization: are trade-offs overrated? Am Nat. 1996;148:S84–107.CrossRef
9.
go back to reference Joshi A, Thompson JN. Trade-offs and the evolution of host specialization. Evol Ecol. 1995;9(1):82–92.CrossRef Joshi A, Thompson JN. Trade-offs and the evolution of host specialization. Evol Ecol. 1995;9(1):82–92.CrossRef
10.
go back to reference Lyimo IN, Ferguson HM. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009;25(4):189–96.CrossRefPubMed Lyimo IN, Ferguson HM. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009;25(4):189–96.CrossRefPubMed
11.
go back to reference Lefèvre T, Gouagna LC, Dabire KR, Elguero E, Fontenille D, Costantini C, et al. Evolutionary lability of odour-mediated host preference by the malaria vector Anopheles gambiae. Trop Med Int Health. 2009;14(2):228–36.CrossRefPubMed Lefèvre T, Gouagna LC, Dabire KR, Elguero E, Fontenille D, Costantini C, et al. Evolutionary lability of odour-mediated host preference by the malaria vector Anopheles gambiae. Trop Med Int Health. 2009;14(2):228–36.CrossRefPubMed
12.
go back to reference Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Ann Rev Entom. 2013;58:433–53.CrossRefPubMed Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Ann Rev Entom. 2013;58:433–53.CrossRefPubMed
13.
go back to reference Tempelis C. Review article: host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entom. 1975;11(6):635–53.CrossRef Tempelis C. Review article: host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entom. 1975;11(6):635–53.CrossRef
14.
15.
go back to reference Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol. 2006;4(4):e82.CrossRefPubMedPubMedCentral Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol. 2006;4(4):e82.CrossRefPubMedPubMedCentral
16.
go back to reference Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, Fonseca DM. Genetic influences on mosquito feeding behavior and the emergence of zoonotic pathogens. Am J Trop Med Hyg. 2007;77(4):667–71.PubMedCrossRef Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P, Fonseca DM. Genetic influences on mosquito feeding behavior and the emergence of zoonotic pathogens. Am J Trop Med Hyg. 2007;77(4):667–71.PubMedCrossRef
17.
go back to reference McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, et al. Evolution of mosquito preference for humans linked to an odorant receptor. Nature. 2014;515(7526):222–7.CrossRefPubMedPubMedCentral McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, et al. Evolution of mosquito preference for humans linked to an odorant receptor. Nature. 2014;515(7526):222–7.CrossRefPubMedPubMedCentral
18.
19.
go back to reference Main BJ, Lee Y, Ferguson HM, Kreppel KS, Kihonda A, Govella NJ, et al. The genetic basis of host preference and resting behavior in the major African malaria vector, Anopheles arabiensis. PLoS Genet. 2016;12(9):e1006303.CrossRefPubMedPubMedCentral Main BJ, Lee Y, Ferguson HM, Kreppel KS, Kihonda A, Govella NJ, et al. The genetic basis of host preference and resting behavior in the major African malaria vector, Anopheles arabiensis. PLoS Genet. 2016;12(9):e1006303.CrossRefPubMedPubMedCentral
20.
go back to reference Harrington LC, Edman JD, Scott TW. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entom. 2001;38(3):411–22.CrossRef Harrington LC, Edman JD, Scott TW. Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entom. 2001;38(3):411–22.CrossRef
21.
go back to reference Lyimo IN, Haydon DT, Russell TL, Mbina KF, Daraja AA, Mbehela EM, et al. The impact of host species and vector control measures on the fitness of African malaria vectors. Proc R Soc B. 2013;280(1754):20122823.CrossRefPubMed Lyimo IN, Haydon DT, Russell TL, Mbina KF, Daraja AA, Mbehela EM, et al. The impact of host species and vector control measures on the fitness of African malaria vectors. Proc R Soc B. 2013;280(1754):20122823.CrossRefPubMed
22.
go back to reference Lyimo I, Keegan S, Ranford-Cartwright L, Ferguson H. The impact of uniform and mixed species blood meals on the fitness of the mosquito vector Anopheles gambiae s.s.: does a specialist pay for diversifying its host species diet? J Evol Biol. 2012;25(3):452–60.CrossRefPubMed Lyimo I, Keegan S, Ranford-Cartwright L, Ferguson H. The impact of uniform and mixed species blood meals on the fitness of the mosquito vector Anopheles gambiae s.s.: does a specialist pay for diversifying its host species diet? J Evol Biol. 2012;25(3):452–60.CrossRefPubMed
24.
go back to reference Bhatt S, Weiss D, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526(7572):207–11.CrossRefPubMedPubMedCentral Bhatt S, Weiss D, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526(7572):207–11.CrossRefPubMedPubMedCentral
25.
go back to reference Hemingway J, Ranson H, Magill A, Kolaczinski J, Fornadel C, Gimnig J, et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016;387(10029):1785–8.CrossRefPubMed Hemingway J, Ranson H, Magill A, Kolaczinski J, Fornadel C, Gimnig J, et al. Averting a malaria disaster: will insecticide resistance derail malaria control? Lancet. 2016;387(10029):1785–8.CrossRefPubMed
26.
go back to reference Gatton ML, Chitnis N, Churcher T, Donnelly MJ, Ghani AC, Godfray HCJ, et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution. 2013;67(4):1218–30.CrossRefPubMedPubMedCentral Gatton ML, Chitnis N, Churcher T, Donnelly MJ, Ghani AC, Godfray HCJ, et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution. 2013;67(4):1218–30.CrossRefPubMedPubMedCentral
27.
go back to reference Stone C, Chitnis N, Gross K. Environmental influences on mosquito foraging and integrated vector management can delay the evolution of behavioral resistance. Evol Appl. 2016;9(3):502–17.CrossRefPubMedPubMedCentral Stone C, Chitnis N, Gross K. Environmental influences on mosquito foraging and integrated vector management can delay the evolution of behavioral resistance. Evol Appl. 2016;9(3):502–17.CrossRefPubMedPubMedCentral
28.
go back to reference Ndenga BA, Mulaya NL, Musaki SK, Shiroko JN, Dongus S, Fillinger U. Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands. Malar J. 2016;15(1):76.CrossRefPubMedPubMedCentral Ndenga BA, Mulaya NL, Musaki SK, Shiroko JN, Dongus S, Fillinger U. Malaria vectors and their blood-meal sources in an area of high bed net ownership in the western Kenya highlands. Malar J. 2016;15(1):76.CrossRefPubMedPubMedCentral
29.
go back to reference Waite JL, Swain S, Lynch PA, Sharma S, Haque MA, Montgomery J, et al. Increasing the potential for malaria elimination by targeting zoophilic vectors. Sci Rep. 2017;7:40551.CrossRefPubMedPubMedCentral Waite JL, Swain S, Lynch PA, Sharma S, Haque MA, Montgomery J, et al. Increasing the potential for malaria elimination by targeting zoophilic vectors. Sci Rep. 2017;7:40551.CrossRefPubMedPubMedCentral
30.
go back to reference Lefèvre T, Gouagna LC, Dabiré KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81(6):1023–9.CrossRefPubMed Lefèvre T, Gouagna LC, Dabiré KR, Elguero E, Fontenille D, Renaud F, et al. Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. Am J Trop Med Hyg. 2009;81(6):1023–9.CrossRefPubMed
31.
go back to reference Beier JC. Frequent blood-feeding and restrictive sugar-feeding behavior enhance the malaria vector potential of Anopheles gambiae sl and An. funestus (Diptera: Culicidae) in western Kenya. J Med Entom. 1996;33(4):613–8.CrossRef Beier JC. Frequent blood-feeding and restrictive sugar-feeding behavior enhance the malaria vector potential of Anopheles gambiae sl and An. funestus (Diptera: Culicidae) in western Kenya. J Med Entom. 1996;33(4):613–8.CrossRef
32.
go back to reference Le Menach A, Takala S, McKenzie FE, Perisse A, Harris A, Flahault A, et al. An elaborated feeding cycle model for reductions in vectorial capacity of night-biting mosquitoes by insecticide-treated nets. Malar J. 2007;6(1):10.CrossRefPubMedPubMedCentral Le Menach A, Takala S, McKenzie FE, Perisse A, Harris A, Flahault A, et al. An elaborated feeding cycle model for reductions in vectorial capacity of night-biting mosquitoes by insecticide-treated nets. Malar J. 2007;6(1):10.CrossRefPubMedPubMedCentral
33.
go back to reference Birget PL, Koella JC. A genetic model of the effects of insecticide-treated bed nets on the evolution of insecticide-resistance. Evol Med Publ Health. 2015;2015(1):205–15.CrossRef Birget PL, Koella JC. A genetic model of the effects of insecticide-treated bed nets on the evolution of insecticide-resistance. Evol Med Publ Health. 2015;2015(1):205–15.CrossRef
34.
go back to reference Brännström Å, Johansson J, von Festenberg N. The hitchhiker’s guide to adaptive dynamics. Games. 2013;4(3):304–28.CrossRef Brännström Å, Johansson J, von Festenberg N. The hitchhiker’s guide to adaptive dynamics. Games. 2013;4(3):304–28.CrossRef
35.
go back to reference Diekmann O. A beginner’s guide to adaptive dynamics. Banach Center Publ. 2004;63:47–86. Diekmann O. A beginner’s guide to adaptive dynamics. Banach Center Publ. 2004;63:47–86.
36.
go back to reference Metz JA, Nisbet RM, Geritz SA. How should we define “fitness” for general ecological scenarios? Trends Ecol Evol. 1992;7(6):198–202.CrossRefPubMed Metz JA, Nisbet RM, Geritz SA. How should we define “fitness” for general ecological scenarios? Trends Ecol Evol. 1992;7(6):198–202.CrossRefPubMed
37.
go back to reference Grant A. Selection pressures on vital rates in density-dependent populations. Proc R Soc B. 1997;264(1380):303–6.CrossRef Grant A. Selection pressures on vital rates in density-dependent populations. Proc R Soc B. 1997;264(1380):303–6.CrossRef
38.
go back to reference Wilbur HM, Rudolf VH. Life-history evolution in uncertain environments: bet hedging in time. Am Nat. 2006;168(3):398–411.PubMed Wilbur HM, Rudolf VH. Life-history evolution in uncertain environments: bet hedging in time. Am Nat. 2006;168(3):398–411.PubMed
39.
go back to reference Rees M, Ellner SP. Evolving integral projection models: evolutionary demography meets eco-evolutionary dynamics. Methods Ecol Evol. 2016;7(2):157–70.CrossRef Rees M, Ellner SP. Evolving integral projection models: evolutionary demography meets eco-evolutionary dynamics. Methods Ecol Evol. 2016;7(2):157–70.CrossRef
40.
go back to reference Briët OJ, Hardy D, Smith TA. Importance of factors determining the effective lifetime of a mass, long-lasting, insecticidal net distribution: a sensitivity analysis. Malar J. 2012;11(1):20.CrossRefPubMedPubMedCentral Briët OJ, Hardy D, Smith TA. Importance of factors determining the effective lifetime of a mass, long-lasting, insecticidal net distribution: a sensitivity analysis. Malar J. 2012;11(1):20.CrossRefPubMedPubMedCentral
41.
go back to reference Ogola E, Villinger J, Mabuka D, Omondi D, Orindi B, Mutunga J, et al. Composition of Anopheles mosquitoes, their blood-meal hosts, and Plasmodium falciparum infection rates in three islands with disparate bed net coverage in Lake Victoria, Kenya. Malar J. 2017;16(1):360.CrossRefPubMedPubMedCentral Ogola E, Villinger J, Mabuka D, Omondi D, Orindi B, Mutunga J, et al. Composition of Anopheles mosquitoes, their blood-meal hosts, and Plasmodium falciparum infection rates in three islands with disparate bed net coverage in Lake Victoria, Kenya. Malar J. 2017;16(1):360.CrossRefPubMedPubMedCentral
42.
go back to reference McGill BJ, Brown JS. Evolutionary game theory and adaptive dynamics of continuous traits. Annu Rev Ecol Evol Syst. 2007;38:403–35.CrossRef McGill BJ, Brown JS. Evolutionary game theory and adaptive dynamics of continuous traits. Annu Rev Ecol Evol Syst. 2007;38:403–35.CrossRef
43.
go back to reference Poisot T, Bever JD, Nemri A, Thrall PH, Hochberg ME. A conceptual framework for the evolution of ecological specialisation. Ecol Lett. 2011;14(9):841–51.CrossRefPubMedPubMedCentral Poisot T, Bever JD, Nemri A, Thrall PH, Hochberg ME. A conceptual framework for the evolution of ecological specialisation. Ecol Lett. 2011;14(9):841–51.CrossRefPubMedPubMedCentral
44.
go back to reference Kelly D, Thompson C. Epidemiology and optimal foraging: modelling the ideal free distribution of insect vectors. Parasitol. 2000;120(3):319–27.CrossRef Kelly D, Thompson C. Epidemiology and optimal foraging: modelling the ideal free distribution of insect vectors. Parasitol. 2000;120(3):319–27.CrossRef
45.
go back to reference Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010;9(1):62.CrossRefPubMedPubMedCentral Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J. 2010;9(1):62.CrossRefPubMedPubMedCentral
46.
go back to reference Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10(1):80.CrossRefPubMedPubMedCentral Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10(1):80.CrossRefPubMedPubMedCentral
47.
go back to reference Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12(1):13.CrossRefPubMedPubMedCentral Mwangangi JM, Mbogo CM, Orindi BO, Muturi EJ, Midega JT, Nzovu J, et al. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12(1):13.CrossRefPubMedPubMedCentral
48.
go back to reference Fornadel CM, Norris LC, Glass GE, Norris DE. Analysis of Anopheles arabiensis blood feeding behavior in southern Zambia during the two years after introduction of insecticide-treated bed nets. Am J Trop Med Hyg. 2010;83(4):848–53.CrossRefPubMedPubMedCentral Fornadel CM, Norris LC, Glass GE, Norris DE. Analysis of Anopheles arabiensis blood feeding behavior in southern Zambia during the two years after introduction of insecticide-treated bed nets. Am J Trop Med Hyg. 2010;83(4):848–53.CrossRefPubMedPubMedCentral
49.
go back to reference Ferriere R, Legendre S. Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory. Phil Trans R Soc B. 2013;368(1610):20120081.CrossRefPubMed Ferriere R, Legendre S. Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory. Phil Trans R Soc B. 2013;368(1610):20120081.CrossRefPubMed
50.
go back to reference Conant J, Fadem P, et al. A community guide to environmental health. Hesperian Foundation; 2008. Conant J, Fadem P, et al. A community guide to environmental health. Hesperian Foundation; 2008.
Metadata
Title
Evolution of host preference in anthropophilic mosquitoes
Authors
Chris Stone
Kevin Gross
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2407-1

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