Cargando…

The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti

BACKGROUND: Aedes aegypti mosquitoes are globally distributed vectors of viruses that impact the health of hundreds of millions of people annually. Mating and blood feeding represent fundamental aspects of mosquito life history that carry important implications for vectorial capacity and for control...

Descripción completa

Detalles Bibliográficos
Autores principales: League, Garrett P., Degner, Ethan C., Pitcher, Sylvie A., Hafezi, Yassi, Tennant, Erica, Cruz, Priscilla C., Krishnan, Raksha S., Garcia Castillo, Stefano S., Alfonso-Parra, Catalina, Avila, Frank W., Wolfner, Mariana F., Harrington, Laura C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8509887/
https://www.ncbi.nlm.nih.gov/pubmed/34591860
http://dx.doi.org/10.1371/journal.pntd.0009815
_version_ 1784582453192556544
author League, Garrett P.
Degner, Ethan C.
Pitcher, Sylvie A.
Hafezi, Yassi
Tennant, Erica
Cruz, Priscilla C.
Krishnan, Raksha S.
Garcia Castillo, Stefano S.
Alfonso-Parra, Catalina
Avila, Frank W.
Wolfner, Mariana F.
Harrington, Laura C.
author_facet League, Garrett P.
Degner, Ethan C.
Pitcher, Sylvie A.
Hafezi, Yassi
Tennant, Erica
Cruz, Priscilla C.
Krishnan, Raksha S.
Garcia Castillo, Stefano S.
Alfonso-Parra, Catalina
Avila, Frank W.
Wolfner, Mariana F.
Harrington, Laura C.
author_sort League, Garrett P.
collection PubMed
description BACKGROUND: Aedes aegypti mosquitoes are globally distributed vectors of viruses that impact the health of hundreds of millions of people annually. Mating and blood feeding represent fundamental aspects of mosquito life history that carry important implications for vectorial capacity and for control strategies. Females transmit pathogens to vertebrate hosts and obtain essential nutrients for eggs during blood feeding. Further, because host-seeking Ae. aegypti females mate with males swarming near hosts, biological crosstalk between these behaviors could be important. Although mating influences nutritional intake in other insects, prior studies examining mating effects on mosquito blood feeding have yielded conflicting results. METHODOLOGY/PRINCIPAL FINDINGS: To resolve these discrepancies, we examined blood-feeding physiology and behavior in virgin and mated females and in virgins injected with male accessory gland extracts (MAG), which induce post-mating changes in female behavior. We controlled adult nutritional status prior to blood feeding by using water- and sugar-fed controls. Our data show that neither mating nor injection with MAG affect Ae. aegypti blood intake, digestion, or feeding avidity for an initial blood meal. However, sugar feeding, a common supplement in laboratory settings but relatively rare in nature, significantly affected all aspects of feeding and may have contributed to conflicting results among previous studies. Further, mating, MAG injection, and sugar intake induced declines in subsequent feedings after an initial blood meal, correlating with egg production and laying. Taking our evaluation to the field, virgin and mated mosquitoes collected in Colombia were equally likely to contain blood at the time of collection. CONCLUSIONS/SIGNIFICANCE: Mating, MAG, and sugar feeding impact a mosquito’s estimated ability to transmit pathogens through both direct and indirect effects on multiple aspects of mosquito biology. Our results highlight the need to consider natural mosquito ecology, including diet, when assessing their physiology and behavior in the laboratory.
format Online
Article
Text
id pubmed-8509887
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-85098872021-10-13 The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti League, Garrett P. Degner, Ethan C. Pitcher, Sylvie A. Hafezi, Yassi Tennant, Erica Cruz, Priscilla C. Krishnan, Raksha S. Garcia Castillo, Stefano S. Alfonso-Parra, Catalina Avila, Frank W. Wolfner, Mariana F. Harrington, Laura C. PLoS Negl Trop Dis Research Article BACKGROUND: Aedes aegypti mosquitoes are globally distributed vectors of viruses that impact the health of hundreds of millions of people annually. Mating and blood feeding represent fundamental aspects of mosquito life history that carry important implications for vectorial capacity and for control strategies. Females transmit pathogens to vertebrate hosts and obtain essential nutrients for eggs during blood feeding. Further, because host-seeking Ae. aegypti females mate with males swarming near hosts, biological crosstalk between these behaviors could be important. Although mating influences nutritional intake in other insects, prior studies examining mating effects on mosquito blood feeding have yielded conflicting results. METHODOLOGY/PRINCIPAL FINDINGS: To resolve these discrepancies, we examined blood-feeding physiology and behavior in virgin and mated females and in virgins injected with male accessory gland extracts (MAG), which induce post-mating changes in female behavior. We controlled adult nutritional status prior to blood feeding by using water- and sugar-fed controls. Our data show that neither mating nor injection with MAG affect Ae. aegypti blood intake, digestion, or feeding avidity for an initial blood meal. However, sugar feeding, a common supplement in laboratory settings but relatively rare in nature, significantly affected all aspects of feeding and may have contributed to conflicting results among previous studies. Further, mating, MAG injection, and sugar intake induced declines in subsequent feedings after an initial blood meal, correlating with egg production and laying. Taking our evaluation to the field, virgin and mated mosquitoes collected in Colombia were equally likely to contain blood at the time of collection. CONCLUSIONS/SIGNIFICANCE: Mating, MAG, and sugar feeding impact a mosquito’s estimated ability to transmit pathogens through both direct and indirect effects on multiple aspects of mosquito biology. Our results highlight the need to consider natural mosquito ecology, including diet, when assessing their physiology and behavior in the laboratory. Public Library of Science 2021-09-30 /pmc/articles/PMC8509887/ /pubmed/34591860 http://dx.doi.org/10.1371/journal.pntd.0009815 Text en © 2021 League et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
League, Garrett P.
Degner, Ethan C.
Pitcher, Sylvie A.
Hafezi, Yassi
Tennant, Erica
Cruz, Priscilla C.
Krishnan, Raksha S.
Garcia Castillo, Stefano S.
Alfonso-Parra, Catalina
Avila, Frank W.
Wolfner, Mariana F.
Harrington, Laura C.
The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti
title The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti
title_full The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti
title_fullStr The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti
title_full_unstemmed The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti
title_short The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti
title_sort impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito aedes aegypti
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8509887/
https://www.ncbi.nlm.nih.gov/pubmed/34591860
http://dx.doi.org/10.1371/journal.pntd.0009815
work_keys_str_mv AT leaguegarrettp theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT degnerethanc theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT pitchersylviea theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT hafeziyassi theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT tennanterica theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT cruzpriscillac theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT krishnanrakshas theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT garciacastillostefanos theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT alfonsoparracatalina theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT avilafrankw theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT wolfnermarianaf theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT harringtonlaurac theimpactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT leaguegarrettp impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT degnerethanc impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT pitchersylviea impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT hafeziyassi impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT tennanterica impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT cruzpriscillac impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT krishnanrakshas impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT garciacastillostefanos impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT alfonsoparracatalina impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT avilafrankw impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT wolfnermarianaf impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti
AT harringtonlaurac impactofmatingandsugarfeedingonbloodfeedingphysiologyandbehaviorinthearbovirusvectormosquitoaedesaegypti