Section: Infections
Topic: Biology of interactions, Health sciences

Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission

10.24072/pcjournal.288 - Peer Community Journal, Volume 3 (2023), article no. e54.

Get full text PDF Peer reviewed and recommended by PCI

The transmission of malaria parasites from mosquito to human is largely determined by the dietary specialization of Anopheles mosquitoes to feed on humans. Few studies have explored the impact of blood meal sources on the fitness of both the parasite and the mosquito. Our study investigated the effects of 3-4 consecutive blood meals from one of four vertebrate species (human, cattle, sheep, or chicken) on several fitness traits, including mosquito feeding rate, blood meal size, susceptibility to wild isolates of Plasmodium falciparum, survival, fecundity, F1 offspring development time, and size. Our findings revealed no significant effect on parasite development. Similarly, parasite exposure had no overall effects on mosquito fitness. However, blood meal type did have a strong impact on mosquito feeding rate, survival, lifetime fecundity, and offspring size. Specifically, mosquitoes that were fed successive chicken blood meals produced fewer eggs and fewer and smaller F1 adults compared to those fed human blood. Combining our results in a theoretical model, we show a decrease in the vectorial capacity of mosquitoes fed chicken or cow blood and an increase in the capacity of those fed sheep blood compared to those fed human blood. These findings emphasize the importance of considering the diversity of blood meal sources in understanding mosquito ecology and their role in the transmission intensity of malaria parasites.

Published online:
DOI: 10.24072/pcjournal.288
Type: Research article
Vantaux, Amélie 1, 2; Moiroux, Nicolas 2, 3; Dabiré, Kounbobr Roch 1, 3; Cohuet, Anna 2, 3; Lefèvre, Thierry 1, 2, 3

1 Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso
2 MIVEGEC, Université de Montpellier, IRD, CNRS, Montpellier, France
3 Laboratoire Mixte International sur les Vecteurs (LAMIVECT), Bobo-Dioulasso, Burkina Faso
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_288,
     author = {Vantaux, Am\'elie and Moiroux, Nicolas and Dabir\'e, Kounbobr Roch and Cohuet, Anna and Lef\`evre, Thierry},
     title = {Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission},
     journal = {Peer Community Journal},
     eid = {e54},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.288},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.288/}
}
TY  - JOUR
AU  - Vantaux, Amélie
AU  - Moiroux, Nicolas
AU  - Dabiré, Kounbobr Roch
AU  - Cohuet, Anna
AU  - Lefèvre, Thierry
TI  - Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.288/
DO  - 10.24072/pcjournal.288
LA  - en
ID  - 10_24072_pcjournal_288
ER  - 
%0 Journal Article
%A Vantaux, Amélie
%A Moiroux, Nicolas
%A Dabiré, Kounbobr Roch
%A Cohuet, Anna
%A Lefèvre, Thierry
%T Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.288/
%R 10.24072/pcjournal.288
%G en
%F 10_24072_pcjournal_288
Vantaux, Amélie; Moiroux, Nicolas; Dabiré, Kounbobr Roch; Cohuet, Anna; Lefèvre, Thierry. Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission. Peer Community Journal, Volume 3 (2023), article  no. e54. doi : 10.24072/pcjournal.288. https://peercommunityjournal.org/articles/10.24072/pcjournal.288/

Peer reviewed and recommended by PCI : 10.24072/pci.infections.100079

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abramoff, M. D.; Magalhaes, P. J.; Ram, S. J. Image processing with ImageJ., Biophotonics International , Volume 11 no. 7, pp. 36-42

[2] Aguilar, R.; Dong, Y.; Warr, E.; Dimopoulos, G. Anopheles infection responses; laboratory models versus field malaria transmission systems, Acta Tropica, Volume 95 (2005) no. 3, pp. 285-291 | DOI

[3] Al-Rashidi, H. S.; Alghamdi, K. M.; Al-Otaibi, W. M.; Al-Solami, H. M.; Mahyoub, J. A. Effects of blood meal sources on the biological characteristics of Aedes aegypti and Culex pipiens (Diptera: Culicidae), Saudi Journal of Biological Sciences, Volume 29 (2022) no. 12 | DOI

[4] Alout, H.; Yameogo, B.; Djogbenou, L. S.; Chandre, F.; Dabire, R. K.; Corbel, V.; Cohuet, A. Interplay Between Plasmodium Infection and Resistance to Insecticides in Vector Mosquitoes, Journal of Infectious Diseases, Volume 210 (2014) no. 9, pp. 1464-1470 | DOI

[5] Alout, H.; Dabiré, R. K.; Djogbénou, L. S.; Abate, L.; Corbel, V.; Chandre, F.; Cohuet, A. Interactive cost of Plasmodium infection and insecticide resistance in the malaria vector Anopheles gambiae, Scientific Reports, Volume 6 (2016) no. 1 | DOI

[6] Atella, G. C.; Bittencourt-Cunha, P. R.; Nunes, R. D.; Shahabuddin, M.; Silva-Neto, M. A. The major insect lipoprotein is a lipid source to mosquito stages of malaria parasite, Acta Tropica, Volume 109 (2009) no. 2, pp. 159-162 | DOI

[7] Atella, G. C.; Silva-Neto, M. A. C.; Golodne, D. M.; Arefin, S.; Shahabuddin, M. Anopheles gambiae lipophorin: Characterization and role in lipid transport to developing oocyte, Insect Biochemistry and Molecular Biology, Volume 36 (2006) no. 5, pp. 375-386 | DOI

[8] Barreaux, A. M. G.; Stone, C. M.; Barreaux, P.; Koella, J. C. The relationship between size and longevity of the malaria vector Anopheles gambiae (s.s.) depends on the larval environment, Parasites & Vectors, Volume 11 (2018) no. 1 | DOI

[9] Barreaux, A. M. G.; Stone, C. M.; Barreaux, P.; Koella, J. C. The relationship between size and longevity of the malaria vector Anopheles gambiae (s.s.) depends on the larval environment, Parasites & Vectors, Volume 11 (2018) no. 1 | DOI

[10] Barry, A.; Bradley, J.; Stone, W.; Guelbeogo, M. W.; Lanke, K.; Ouedraogo, A.; Soulama, I.; Nébié, I.; Serme, S. S.; Grignard, L.; Patterson, C.; Wu, L.; Briggs, J. J.; Janson, O.; Awandu, S. S.; Ouedraogo, M.; Tarama, C. W.; Kargougou, D.; Zongo, S.; Sirima, S. B.; Marti, M.; Drakeley, C.; Tiono, A. B.; Bousema, T. Higher gametocyte production and mosquito infectivity in chronic compared to incident Plasmodium falciparum infections, Nature Communications, Volume 12 (2021) no. 1 | DOI

[11] Beier, J. C. Malaria parasite development in mosquitoes, Annual Review of Entomology, Volume 43 (1998) no. 1, pp. 519-543 | DOI

[12] Billker, O.; Lindo, V.; Panico, M.; Etienne, A. E.; Paxton, T.; Dell, A.; Rogers, M.; Sinden, R. E.; Morris, H. R. Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito, Nature, Volume 392 (1998) no. 6673, pp. 289-292 | DOI

[13] Bousema, T.; Dinglasan, R. R.; Morlais, I.; Gouagna, L. C.; van Warmerdam, T.; Awono-Ambene, P. H.; Bonnet, S.; Diallo, M.; Coulibaly, M.; Tchuinkam, T.; Mulder, B.; Targett, G.; Drakeley, C.; Sutherland, C.; Robert, V.; Doumbo, O.; Touré, Y.; Graves, P. M.; Roeffen, W.; Sauerwein, R.; Birkett, A.; Locke, E.; Morin, M.; Wu, Y.; Churcher, T. S. Mosquito Feeding Assays to Determine the Infectiousness of Naturally Infected Plasmodium falciparum Gametocyte Carriers, PLoS ONE, Volume 7 (2012) no. 8 | DOI

[14] Brackney, D. E.; LaReau, J. C.; Smith, R. C. Frequency matters: How successive feeding episodes by blood-feeding insect vectors influences disease transmission, PLOS Pathogens, Volume 17 (2021) no. 6 | DOI

[15] Brady, O. J.; Godfray, H. C. J.; Tatem, A. J.; Gething, P. W.; Cohen, J. M.; McKenzie, F. E.; Perkins, T. A.; Reiner, R. C.; Tusting, L. S.; Sinka, M. E.; Moyes, C. L.; Eckhoff, P. A.; Scott, T. W.; Lindsay, S. W.; Hay, S. I.; Smith, D. L. Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination, Transactions of The Royal Society of Tropical Medicine and Hygiene, Volume 110 (2016) no. 2, pp. 107-117 | DOI

[16] Briegel, H.; Hefti, M.; DiMarco, E. Lipid metabolism during sequential gonotrophic cycles in large and small female Aedes aegypti, Journal of Insect Physiology, Volume 48 (2002) no. 5, pp. 547-554 | DOI

[17] Briegel, H. Fecundity, Metabolism, and Body Size in Anopheles (Diptera: Culicidae), Vectors of Malaria, Journal of Medical Entomology, Volume 27 (1990) no. 5, pp. 839-850 | DOI

[18] Brooks, M.; Kristensen, K.; Benthem, K.; Magnusson, A.; Berg, C.; Nielsen, A.; Skaug, H.; Mächler, M.; Bolker, B. glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling, The R Journal, Volume 9 (2017) no. 2 | DOI

[19] Caputo, B.; Nwakanma, D.; Jawara, M.; Adiamoh, M.; Dia, I.; Konate, L.; Petrarca, V.; Conway, D. J.; della Torre, A. Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s.s, Malaria Journal, Volume 7 (2008) no. 1 | DOI

[20] Cheon, H.-M.; Shin, S. W.; Bian, G.; Park, J.-H.; Raikhel, A. S. Regulation of Lipid Metabolism Genes, Lipid Carrier Protein Lipophorin, and Its Receptor during Immune Challenge in the Mosquito Aedes aegypti, Journal of Biological Chemistry, Volume 281 (2006) no. 13, pp. 8426-8435 | DOI

[21] Clements, A. N. The biology of mosquitoes. Development, nutrition and reproduction, Chapman & hall., London, 1992, 532 pages

[22] Coetzee, M.; Hunt, R. H.; Wilkerson, R.; Torre, A. D.; Coulibaly, M. B.; Besansky, N. J. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex, Zootaxa, Volume 3619 (2013) no. 3, pp. 246-274 | DOI

[23] Costantini, C.; Sagnon, N.; della Torre, A.; Coluzzi, M. Mosquito behavioural aspects of vector-human interactions in the Anopheles gambiae complex, Parassitologia, Volume 41 (1999) no. 1-3, pp. 209-217

[24] Crawley, M. J. The R Book, John Wiley & Sons, Ltd, Chichester, UK, 2007 | DOI

[25] De Smet, W. H. The total protein content in the blood serum of vertebrates, Acta Zool Pathol Antverp, Volume 70 (1978), pp. 35-56

[26] Donnelly, B.; Berrang-Ford, L.; Ross, N. A.; Michel, P. A systematic, realist review of zooprophylaxis for malaria control, Malaria Journal, Volume 14 (2015) no. 1 | DOI

[27] Edman, J. D.; Scott, T. W. Host defensive behaviour and the feeding success of mosquitoes, International Journal of Tropical Insect Science, Volume 8 (1987) no. 4-5-6, pp. 617-622 | DOI

[28] Emami, S. N.; Ranford-Cartwright, L. C.; Ferguson, H. M. The transmission potential of malaria-infected mosquitoes (An.gambiae-Keele, An.arabiensis-Ifakara) is altered by the vertebrate blood type they consume during parasite development, Scientific Reports, Volume 7 (2017) no. 1 | DOI

[29] Ferguson, H. M.; Read, A. F. Genetic and environmental determinants of malaria parasite virulence in mosquitoes, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1497, pp. 1217-1224 | DOI

[30] Ferguson, H. M.; Read, A. F. Why is the effect of malaria parasites on mosquito survival still unresolved?, Trends in Parasitology, Volume 18 (2002) no. 6, pp. 256-261 | DOI

[31] Fikrig, K.; Martin, E.; Dang, S.; St Fleur, K.; Goldsmith, H.; Qu, S.; Rosenthal, H.; Pitcher, S.; Harrington, L. C. The Effects of Host Availability and Fitness on Aedes albopictus Blood Feeding Patterns in New York, The American Journal of Tropical Medicine and Hygiene, Volume 106 (2022) no. 1, pp. 320-331 | DOI

[32] Flatt, T. Survival costs of reproduction in Drosophila, Experimental Gerontology, Volume 46 (2011) no. 5, pp. 369-375 | DOI

[33] Flatt, T. Life-History Evolution and the Genetics of Fitness Components in Drosophila melanogaster, Genetics, Volume 214 (2020) no. 1, pp. 3-48 | DOI

[34] Foster, W. Chapter 7: Behavioural ecology of plant-mosquito relations, Sensory ecology of disease vectors, Wageningen Academic Publishers, The Netherlands, 2022, pp. 171-234 | DOI

[35] Grignard, L.; Gonçalves, B. P.; Early, A. M.; Daniels, R. F.; Tiono, A. B.; Guelbéogo, W. M.; Ouédraogo, A.; van Veen, E. M.; Lanke, K.; Diarra, A.; Nebie, I.; Sirima, S. B.; Targett, G. A.; Volkman, S. K.; Neafsey, D. E.; Wirth, D. F.; Bousema, T.; Drakeley, C. Transmission of molecularly undetectable circulating parasite clones leads to high infection complexity in mosquitoes post feeding, International Journal for Parasitology, Volume 48 (2018) no. 8, pp. 671-677 | DOI

[36] Grimm, V.; Berger, U.; DeAngelis, D. L.; Polhill, J. G.; Giske, J.; Railsback, S. F. The ODD protocol: A review and first update, Ecological Modelling, Volume 221 (2010) no. 23, pp. 2760-2768 | DOI

[37] Habtewold, T.; Sharma, A. A.; Wyer, C. A. S.; Masters, E. K. G.; Windbichler, N.; Christophides, G. K. Plasmodium oocysts respond with dormancy to crowding and nutritional stress, Scientific Reports, Volume 11 (2021) no. 1 | DOI

[38] Habtewold, T.; Tapanelli, S.; Masters, E. K. G.; Windbichler, N.; Christophides, G. K. The circadian clock modulates Anopheles gambiae infection with Plasmodium falciparum, PLOS ONE, Volume 17 (2022) no. 12 | DOI

[39] Hasyim, H.; Dhimal, M.; Bauer, J.; Montag, D.; Groneberg, D. A.; Kuch, U.; Müller, R. Does livestock protect from malaria or facilitate malaria prevalence? A cross-sectional study in endemic rural areas of Indonesia, Malaria Journal, Volume 17 (2018) no. 1 | DOI

[40] Hawkey, C. M.; Bennett, P. M.; Gascoyne, S. C.; Hart, M. G.; Kirkwood, J. K. Erythrocyte size, number and haemoglobin content in vertebrates, British Journal of Haematology, Volume 77 (1991) no. 3, pp. 392-397 | DOI

[41] Hien, D. F. d. S.; Dabiré, K. R.; Roche, B.; Diabaté, A.; Yerbanga, R. S.; Cohuet, A.; Yameogo, B. K.; Gouagna, L.-C.; Hopkins, R. J.; Ouedraogo, G. A.; Simard, F.; Ouedraogo, J.-B.; Ignell, R.; Lefevre, T. Plant-Mediated Effects on Mosquito Capacity to Transmit Human Malaria, PLOS Pathogens, Volume 12 (2016) no. 8 | DOI

[42] Hsu, C.-H.; Posegga, O.; Fischbach, K.; Engelhardt, H. Examining the trade-offs between human fertility and longevity over three centuries using crowdsourced genealogy data, PLOS ONE, Volume 16 (2021) no. 8 | DOI

[43] Kemibala, E. E.; Mafra-Neto, A.; Dekker, T.; Saroli, J.; Silva, R.; Philbert, A.; Nghabi, K.; Mboera, L. E. G. A zooprophylaxis strategy using l-lactic acid (Abate) to divert host-seeking malaria vectors from human host to treated non-host animals, Malaria Journal, Volume 19 (2020) no. 1 | DOI

[44] Khaligh, F. G.; Jafari, A.; Silivanova, E.; Levchenko, M.; Rahimi, B.; Gholizadeh, S. Endectocides as a complementary intervention in the malaria control program: a systematic review, Systematic Reviews, Volume 10 (2021) no. 1 | DOI

[45] Kittayapong, P.; Edman, J. D.; Harrison, B. A.; Delorme, D. R. Female Body Size, Parity, and Malaria Infection of Anopheles maculatus (Diptera: Culicidae) in Peninsular Malaysia, Journal of Medical Entomology, Volume 29 (1992) no. 3, pp. 379-383 | DOI

[46] Kwon, H.; Simões, M. L.; Reynolds, R. A.; Dimopoulos, G.; Smith, R. C. Additional Feeding Reveals Differences in Immune Recognition and Growth of Plasmodium Parasites in the Mosquito Host, mSphere, Volume 6 (2021) no. 2 | DOI

[47] Lahondère, C.; Lazzari, C. R. Mosquitoes Cool Down during Blood Feeding to Avoid Overheating, Current Biology, Volume 22 (2012) no. 1, pp. 40-45 | DOI

[48] Lalubin, F.; Delédevant, A.; Glaizot, O.; Christe, P. Natural malaria infection reduces starvation resistance of nutritionally stressed mosquitoes, Journal of Animal Ecology, Volume 83 (2014) no. 4, pp. 850-857 | DOI

[49] Lambrechts, L.; Chavatte, J.-M.; Snounou, G.; Koella, J. C. Environmental influence on the genetic basis of mosquito resistance to malaria parasites, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1593, pp. 1501-1506 | DOI

[50] Lefèvre, T.; Gouagna, L.-C.; Dabire, K. R.; Elguero, E.; Fontenille, D.; Costantini, C.; Thomas, F. Evolutionary lability of odour-mediated host preference by the malaria vectorAnopheles gambiae, Tropical Medicine & International Health, Volume 14 (2009) no. 2, pp. 228-236 | DOI

[51] Lefèvre, T.; Thomas, F.; Renaud, F.; Elguero, E.; Fontenille, D.; Gouagna, L.-C.; Dabiré, K. R.; Costantini, C. Beyond Nature and Nurture: Phenotypic Plasticity in Blood-Feeding Behavior of Anopheles gambiae s.s. When Humans Are Not Readily Accessible, The American Journal of Tropical Medicine and Hygiene, Volume 81 (2009) no. 6, pp. 1023-1029 | DOI

[52] Lemasson, J.-J.; Fontenille, D.; Lochouarn, L.; Dia, I.; Simard, F.; Ba, K.; Diop, A.; Diatta, M.; Molez, J.-F. Comparison of Behavior and Vector Efficiency of Anopheles gambiae and An. arabiensis (Diptera: Culicidae) in Barkedji, a Sahelian Area of Senegal, Journal of Medical Entomology, Volume 34 (1997) no. 4, pp. 396-403 | DOI

[53] Lenth, R. V. emmeans: Estimated Marginal Means, aka Least-Squares Means, R package version 1.7.2, 2022 (https://CRAN.R-project.org/package=emmeans)

[54] Lyimo, E. O.; Koella, J. C. Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum, Parasitology, Volume 104 (1992) no. 2, pp. 233-237 | DOI

[55] Lyimo, E. O.; Takken, W. Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania, Medical and Veterinary Entomology, Volume 7 (1993) no. 4, pp. 328-332 | DOI

[56] Lyimo, I. N.; Keegan, S. P.; Ranford-Cartwright, L. C.; Ferguson, H. M. 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?, Journal of Evolutionary Biology, Volume 25 (2012) no. 3, pp. 452-460 | DOI

[57] Lyimo, I. N.; Haydon, D. T.; Mbina, K. F.; Daraja, A. A.; Mbehela, E. M.; Reeve, R.; Ferguson, H. M. The fitness of African malaria vectors in the presence and limitation of host behaviour, Malaria Journal, Volume 11 (2012) no. 1 | DOI

[58] Lyimo, I. N.; Ferguson, H. M. Ecological and evolutionary determinants of host species choice in mosquito vectors, Trends in Parasitology, Volume 25 (2009) no. 4, pp. 189-196 | DOI

[59] Lyimo, I. N.; Haydon, D. T.; Russell, T. L.; Mbina, K. F.; Daraja, A. A.; Mbehela, E. M.; Reeve, R.; Ferguson, H. M. The impact of host species and vector control measures on the fitness of African malaria vectors, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1754 | DOI

[60] MacDonald, G. .. The epidemiology and control of malaria, Oxford University Press, London, 1957

[61] Mollahosseini, A.; Rossignol, M.; Pennetier, C.; Cohuet, A.; Anjos, A. d.; Chandre, F.; Shahbazkia, H. R. A user-friendly software to easily count Anopheles egg batches, Parasites & Vectors, Volume 5 (2012) no. 1 | DOI

[62] Morassin, B.; Magnaval, J. F.; Berry, A.; Fabre, R. One year's experience with the polymerase chain reaction as a routine method for the diagnosis of imported malaria., The American Journal of Tropical Medicine and Hygiene, Volume 66 (2002) no. 5, pp. 503-508 | DOI

[63] Oliver, S. V.; Brooke, B. D. The effect of multiple blood-feeding on the longevity and insecticide resistant phenotype in the major malaria vector Anopheles arabiensis (Diptera: Culicidae), Parasites & Vectors, Volume 7 (2014) no. 1 | DOI

[64] Oliver, S. V.; Lyons, C. L.; Brooke, B. D. The effect of blood feeding on insecticide resistance intensity and adult longevity in the major malaria vector Anopheles funestus (Diptera: Culicidae), Scientific Reports, Volume 12 (2022) no. 1 | DOI

[65] Ouédraogo, A.; Guelbéogo, W.; Cohuet, A.; Morlais, I.; King, J.; Gonçalves, B.; Bastiaens, G.; Thiombiano, F.; Sattabongkot, J.; Wu, Y.; Coulibaly, M.; Ibrahima, B.; Jones, S.; Drakeley, C.; Dinglasan, R.; Bousema, T. A protocol for membrane feeding assays to determine the infectiousness of P. falciparum naturally infected individuals to Anopheles gambiae, Malaria World Journal, Volume 4 (2013) no. 16

[66] O’Donnell, A. J.; Rund, S. S. C.; Reece, S. E. Time-of-day of blood-feeding: effects on mosquito life history and malaria transmission, Parasites & Vectors, Volume 12 (2019) no. 1 | DOI

[67] Pathak, A. K.; Shiau, J. C.; de Freitas, C. R. S.; Kyle, D. E. Blood meals from ‘dead-end’ vertebrate hosts enhance transmission potential of malaria-infected mosquitoes, bioRxiv (2022) | DOI

[68] Phasomkusolsil, S.; Tawong, J.; Monkanna, N.; Pantuwatana, K.; Damdangdee, N.; Khongtak, W.; Kertmanee, Y.; Evans, B. P.; Schuster, A. L. Maintenance of mosquito vectors: effects of blood source on feeding, survival, fecundity, and egg hatching rates, Journal of Vector Ecology, Volume 38 (2013) no. 1, pp. 38-45 | DOI

[69] Pigeault, R.; Villa, M. Long-term pathogenic response to Plasmodium relictum infection in Culex pipiens mosquito, PLOS ONE, Volume 13 (2018) no. 2 | DOI

[70] Ponnudurai, T.; Lensen, A.; van Gemert, G.; Bensink, M.; Bolmer, M.; Meuwissen, J. Sporozoite load of mosquitoes infected with Plasmodium falciparum, Transactions of the Royal Society of Tropical Medicine and Hygiene, Volume 83 (1989) no. 1, pp. 67-70 | DOI

[71] Pooda, H. S.; Rayaisse, J.-B.; Hien, D. F. d. S.; Lefèvre, T.; Yerbanga, S. R.; Bengaly, Z.; Dabiré, R. K.; Belem, A. M. G.; Sidibé, I.; Solano, P.; Mouline, K. Administration of ivermectin to peridomestic cattle: a promising approach to target the residual transmission of human malaria, Malaria Journal, Volume 14 (2015) no. 1 | DOI

[72] R Core Team R: A language and environment for statistical computing. , Vienna, Austria, R Foundation for Statistical Computing, 2020 (http://www.r-project.org/index.html)

[73] Rono, M. K.; Whitten, M. M. A.; Oulad-Abdelghani, M.; Levashina, E. A.; Marois, E. The Major Yolk Protein Vitellogenin Interferes with the Anti-Plasmodium Response in the Malaria Mosquito Anopheles gambiae, PLoS Biology, Volume 8 (2010) no. 7 | DOI

[74] Roux, O.; Vantaux, A.; Roche, B.; Yameogo, K. B.; Dabiré, K. R.; Diabaté, A.; Simard, F.; Lefèvre, T. Evidence for carry-over effects of predator exposure on pathogen transmission potential, Proceedings of the Royal Society B: Biological Sciences, Volume 282 (2015) no. 1821 | DOI

[75] Sangare, I.; Dabire, R.; Yameogo, B.; Da, D.; Michalakis, Y.; Cohuet, A. Stress dependent infection cost of the human malaria agent Plasmodium falciparum on its natural vector Anopheles coluzzii, Infection, Genetics and Evolution, Volume 25 (2014), pp. 57-65 | DOI

[76] Sangare, I.; Michalakis, Y.; Yameogo, B.; Dabire, R.; Morlais, I.; Cohuet, A. Studying fitness cost of Plasmodium falciparum infection in malaria vectors: validation of an appropriate negative control, Malaria Journal, Volume 12 (2013) no. 1 | DOI

[77] Santiago-Alarcon, D. What you eat can eliminate you: bloodmeal sources and mosquito fitness, Peer Community In Infections (2023) | DOI

[78] Santolamazza, F.; Mancini, E.; Simard, F.; Qi, Y.; Tu, Z.; della Torre, A. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms, Malaria Journal, Volume 7 (2008) no. 1 | DOI

[79] Saul, A. J.; Graves, P. M.; Kay, B. H. A Cyclical Feeding Model for Pathogen Transmission and Its Application to Determine Vectorial Capacity from Vector Infection Rates, The Journal of Applied Ecology, Volume 27 (1990) no. 1 | DOI

[80] Schneider, P.; Rund, S. S. C.; Smith, N. L.; Prior, K. F.; O'Donnell, A. J.; Reece, S. E. Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes, Proceedings of the Royal Society B: Biological Sciences, Volume 285 (2018) no. 1888 | DOI

[81] Seaman, J. A.; Alout, H.; Meyers, J. I.; Stenglein, M. D.; Dabiré, R. K.; Lozano-Fuentes, S.; Burton, T. A.; Kuklinski, W. S.; Black, W. C.; Foy, B. D. Age and prior blood feeding of Anopheles gambiae influences their susceptibility and gene expression patterns to ivermectin-containing blood meals, BMC Genomics, Volume 16 (2015) no. 1 | DOI

[82] Shaw, W. R.; Holmdahl, I. E.; Itoe, M. A.; Werling, K.; Marquette, M.; Paton, D. G.; Singh, N.; Buckee, C. O.; Childs, L. M.; Catteruccia, F. Multiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential, PLOS Pathogens, Volume 16 (2020) no. 12 | DOI

[83] Shaw, W. R.; Marcenac, P.; Catteruccia, F. Plasmodium development in Anopheles: a tale of shared resources, Trends in Parasitology, Volume 38 (2022) no. 2, pp. 124-135 | DOI

[84] Smith, D. L.; Ellis McKenzie, F. Malaria Journal, 3 (2004) no. 1 | DOI

[85] Sondo, P.; Derra, K.; Rouamba, T.; Nakanabo Diallo, S.; Taconet, P.; Kazienga, A.; Ilboudo, H.; Tahita, M. C.; Valéa, I.; Sorgho, H.; Lefèvre, T.; Tinto, H. Determinants of Plasmodium falciparum multiplicity of infection and genetic diversity in Burkina Faso, Parasites & Vectors, Volume 13 (2020) no. 1 | DOI

[86] Sousa, C. A.; Pinto, J.; Almeida, P. G.; Ferreira, C.; Do Rosário, V. E.; Charlwood, J. D. Dogs as a Favored Host Choice of Anopheles gambiae sensu stricto (Diptera: Culicidae) of São Tomé, West Africa, Journal of Medical Entomology, Volume 38 (2001) no. 1, pp. 122-125 | DOI

[87] Stearns, S. C. The evolution of life histories, Oxford University Press, Oxford, 1992, 262 pages

[88] Takken, W.; Verhulst, N. O. Host Preferences of Blood-Feeding Mosquitoes, Annual Review of Entomology, Volume 58 (2013) no. 1, pp. 433-453 | DOI

[89] Therneau, T. M. coxme: Mixed Effects Cox Models. R package version 2.2-16., 2020 (http://CRAN.R-project.org/package=coxme)

[90] Tripet, F.; Aboagye-Antwi, F.; Hurd, H. Ecological immunology of mosquito–malaria interactions, Trends in Parasitology, Volume 24 (2008) no. 5, pp. 219-227 | DOI

[91] Van Handel, E.; Day, J. F. Correlation between wing length and protein content of mosquitoes, J Am Mosq Control Assoc (5), Volume 2 (1989), pp. 180-182

[92] Vantaux, A. Datasets and R script to replicate the statistical analyses from the article entitled Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission [Data set], Zenodo, 2023 | DOI

[93] Vantaux, A. Datasets and R script to replicate the theoretical modeling from the article entitled Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission [Data set], Zenodo, 2023 | DOI

[94] Vantaux, A.; Lefèvre, T.; Cohuet, A.; Dabiré, K. R.; Roche, B.; Roux, O. Larval nutritional stress affects vector life history traits and human malaria transmission, Scientific Reports, Volume 6 (2016) no. 1 | DOI

[95] Vantaux, A.; Lefèvre, T.; Dabiré, K.; Cohuet, A. Individual experience affects host choice in malaria vector mosquitoes, Parasites & Vectors, Volume 7 (2014) no. 1 | DOI

[96] Vantaux, A.; Ouattarra, I.; Lefèvre, T.; Dabiré, K. R. Effects of larvicidal and larval nutritional stresses on Anopheles gambiae development, survival and competence for Plasmodium falciparum, Parasites & Vectors, Volume 9 (2016) no. 1 | DOI

[97] Vantaux, A.; Yao, F.; Hien, D. F.; Guissou, E.; Yameogo, B. K.; Gouagna, L.-C.; Fontenille, D.; Renaud, F.; Simard, F.; Constantini, C.; Thomas, F.; Mouline, K.; Roche, B.; Cohuet, A.; Dabiré, K. R.; Lefèvre, T. Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum, Peer Community Journal, Volume 1 (2021) | DOI

[98] Vantaux, A.; de Sales Hien, D. F.; Yameogo, B.; Dabiré, K. R.; Thomas, F.; Cohuet, A.; Lefèvre, T. Host-seeking behaviors of mosquitoes experimentally infected with sympatric field isolates of the human malaria parasite Plasmodium falciparum: no evidence for host manipulation, Frontiers in Ecology and Evolution, Volume 3 (2015) | DOI

[99] Vaughan, D.; Dancho, M. furrr: Apply Mapping Functions in Parallel using Futures. R package version 0.2.3, , 2021 (https://CRAN.R-project.org/package=furrr)

[100] Vézilier, J.; Nicot, A.; Gandon, S.; Rivero, A. Plasmodium infection decreases fecundity and increases survival of mosquitoes, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1744, pp. 4033-4041 | DOI

[101] Wickham, H.; Averick, M.; Bryan, J.; Chang, W.; McGowan, L.; François, R.; Grolemund, G.; Hayes, A.; Henry, L.; Hester, J.; Kuhn, M.; Pedersen, T.; Miller, E.; Bache, S.; Müller, K.; Ooms, J.; Robinson, D.; Seidel, D.; Spinu, V.; Takahashi, K.; Vaughan, D.; Wilke, C.; Woo, K.; Yutani, H. Welcome to the Tidyverse, Journal of Open Source Software, Volume 4 (2019) no. 43 | DOI

[102] Wintrobe, M. M. Variations in size and hemoglobin content of erythrocytes in the blood of various vertebrates, Folia Haematol, Volume 51 (1933), pp. 32-49

[103] Zera, A. J.; Harshman, L. G. The Physiology of Life History Trade-Offs in Animals, Annual Review of Ecology and Systematics, Volume 32 (2001) no. 1, pp. 95-126 | DOI

Cited by Sources: