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Susceptibility of Anopheles stephensi to Plasmodium gallinaceum: a trait of the mosquito, the parasite, and the environment.

Hume JC, Hamilton H, Lee KL, Lehmann T - PLoS ONE (2011)

Bottom Line: Notably, the environment contributed 28%.These estimates are relevant only to the particular system under study, but this experimental design could be useful for other parasite-host systems.The prospects and limitations of the genetic manipulation of vector populations to render the vector resistant to the parasite are better considered on the basis of this framework.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, United States of America.

ABSTRACT

Background: Vector susceptibility to Plasmodium infection is treated primarily as a vector trait, although it is a composite trait expressing the joint occurrence of the parasite and the vector with genetic contributions of both. A comprehensive approach to assess the specific contribution of genetic and environmental variation on "vector susceptibility" is lacking. Here we developed and implemented a simple scheme to assess the specific contributions of the vector, the parasite, and the environment to "vector susceptibility." To the best of our knowledge this is the first study that employs such an approach.

Methodology/principal findings: We conducted selection experiments on the vector (while holding the parasite "constant") and on the parasite (while holding the vector "constant") to estimate the genetic contributions of the mosquito and the parasite to the susceptibility of Anopheles stephensi to Plasmodium gallinaceum. We separately estimated the realized heritability of (i) susceptibility to parasite infection by the mosquito vector and (ii) parasite compatibility (transmissibility) with the vector while controlling the other. The heritabilities of vector and the parasite were higher for the prevalence, i.e., fraction of infected mosquitoes, than the corresponding heritabilities of parasite load, i.e., the number of oocysts per mosquito.

Conclusions: The vector's genetics (heritability) comprised 67% of "vector susceptibility" measured by the prevalence of mosquitoes infected with P. gallinaceum oocysts, whereas the specific contribution of parasite genetics (heritability) to this trait was only 5%. Our parasite source might possess minimal genetic diversity, which could explain its low heritability (and the high value of the vector). Notably, the environment contributed 28%. These estimates are relevant only to the particular system under study, but this experimental design could be useful for other parasite-host systems. The prospects and limitations of the genetic manipulation of vector populations to render the vector resistant to the parasite are better considered on the basis of this framework.

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Selection protocol for increasing vector susceptibility.Schematic illustrating selection protocol for increased vector susceptibility (nVC) in An. stephensi infected with P. gallinaceum. (1) An. stephensi colony mosquitoes randomly chosen for the selection experiment; (2) feed on P. gallinaceum infected chicken (side by side with Ae. aegypti, used as positive control); (3) Mosquitoes separated out individually on day 5 p.i for oviposition. On day 6 p.i., a subset of the females that laid eggs (50<N<200) were dissected for determination of oocyst count in their midgut i.,e., red denotes infected and black denotes uninfected. (4) Eggs set up from all infected mosquitoes (red) to generate the next generation of the selected line and from a matching number of unknown (not dissected) females to generate the next generation of the control line (gray). (5) Larvae reared to adults for next cycle. (6) Offspring of the selected and control line fed again on an infected chicken. Processes 2–6 repeated for subsequent generations.
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pone-0020156-g001: Selection protocol for increasing vector susceptibility.Schematic illustrating selection protocol for increased vector susceptibility (nVC) in An. stephensi infected with P. gallinaceum. (1) An. stephensi colony mosquitoes randomly chosen for the selection experiment; (2) feed on P. gallinaceum infected chicken (side by side with Ae. aegypti, used as positive control); (3) Mosquitoes separated out individually on day 5 p.i for oviposition. On day 6 p.i., a subset of the females that laid eggs (50<N<200) were dissected for determination of oocyst count in their midgut i.,e., red denotes infected and black denotes uninfected. (4) Eggs set up from all infected mosquitoes (red) to generate the next generation of the selected line and from a matching number of unknown (not dissected) females to generate the next generation of the control line (gray). (5) Larvae reared to adults for next cycle. (6) Offspring of the selected and control line fed again on an infected chicken. Processes 2–6 repeated for subsequent generations.

Mentions: Mosquitoes were reared under 28°C, 75% humidity, and 12 hour light/dark cycle. For the selection experiment, 3–8 days old female mosquitoes were first separated out into groups of 300–400 individuals per cage. Experiments comprised of mosquitoes which were 1–3 days apart in age. Mosquitoes were maintained on distilled water for 12–15 hours prior to feeding on a restrained infected chicken (parasitemias normally between 10–20% with gametocytes present) for up to 45 minutes depending on feeding rate (90% of females typically feed within 20 minutes). A few hours post-feeding, unfed females were removed. A schematic describing the selection process is shown in Figure 1.


Susceptibility of Anopheles stephensi to Plasmodium gallinaceum: a trait of the mosquito, the parasite, and the environment.

Hume JC, Hamilton H, Lee KL, Lehmann T - PLoS ONE (2011)

Selection protocol for increasing vector susceptibility.Schematic illustrating selection protocol for increased vector susceptibility (nVC) in An. stephensi infected with P. gallinaceum. (1) An. stephensi colony mosquitoes randomly chosen for the selection experiment; (2) feed on P. gallinaceum infected chicken (side by side with Ae. aegypti, used as positive control); (3) Mosquitoes separated out individually on day 5 p.i for oviposition. On day 6 p.i., a subset of the females that laid eggs (50<N<200) were dissected for determination of oocyst count in their midgut i.,e., red denotes infected and black denotes uninfected. (4) Eggs set up from all infected mosquitoes (red) to generate the next generation of the selected line and from a matching number of unknown (not dissected) females to generate the next generation of the control line (gray). (5) Larvae reared to adults for next cycle. (6) Offspring of the selected and control line fed again on an infected chicken. Processes 2–6 repeated for subsequent generations.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111409&req=5

pone-0020156-g001: Selection protocol for increasing vector susceptibility.Schematic illustrating selection protocol for increased vector susceptibility (nVC) in An. stephensi infected with P. gallinaceum. (1) An. stephensi colony mosquitoes randomly chosen for the selection experiment; (2) feed on P. gallinaceum infected chicken (side by side with Ae. aegypti, used as positive control); (3) Mosquitoes separated out individually on day 5 p.i for oviposition. On day 6 p.i., a subset of the females that laid eggs (50<N<200) were dissected for determination of oocyst count in their midgut i.,e., red denotes infected and black denotes uninfected. (4) Eggs set up from all infected mosquitoes (red) to generate the next generation of the selected line and from a matching number of unknown (not dissected) females to generate the next generation of the control line (gray). (5) Larvae reared to adults for next cycle. (6) Offspring of the selected and control line fed again on an infected chicken. Processes 2–6 repeated for subsequent generations.
Mentions: Mosquitoes were reared under 28°C, 75% humidity, and 12 hour light/dark cycle. For the selection experiment, 3–8 days old female mosquitoes were first separated out into groups of 300–400 individuals per cage. Experiments comprised of mosquitoes which were 1–3 days apart in age. Mosquitoes were maintained on distilled water for 12–15 hours prior to feeding on a restrained infected chicken (parasitemias normally between 10–20% with gametocytes present) for up to 45 minutes depending on feeding rate (90% of females typically feed within 20 minutes). A few hours post-feeding, unfed females were removed. A schematic describing the selection process is shown in Figure 1.

Bottom Line: Notably, the environment contributed 28%.These estimates are relevant only to the particular system under study, but this experimental design could be useful for other parasite-host systems.The prospects and limitations of the genetic manipulation of vector populations to render the vector resistant to the parasite are better considered on the basis of this framework.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, United States of America.

ABSTRACT

Background: Vector susceptibility to Plasmodium infection is treated primarily as a vector trait, although it is a composite trait expressing the joint occurrence of the parasite and the vector with genetic contributions of both. A comprehensive approach to assess the specific contribution of genetic and environmental variation on "vector susceptibility" is lacking. Here we developed and implemented a simple scheme to assess the specific contributions of the vector, the parasite, and the environment to "vector susceptibility." To the best of our knowledge this is the first study that employs such an approach.

Methodology/principal findings: We conducted selection experiments on the vector (while holding the parasite "constant") and on the parasite (while holding the vector "constant") to estimate the genetic contributions of the mosquito and the parasite to the susceptibility of Anopheles stephensi to Plasmodium gallinaceum. We separately estimated the realized heritability of (i) susceptibility to parasite infection by the mosquito vector and (ii) parasite compatibility (transmissibility) with the vector while controlling the other. The heritabilities of vector and the parasite were higher for the prevalence, i.e., fraction of infected mosquitoes, than the corresponding heritabilities of parasite load, i.e., the number of oocysts per mosquito.

Conclusions: The vector's genetics (heritability) comprised 67% of "vector susceptibility" measured by the prevalence of mosquitoes infected with P. gallinaceum oocysts, whereas the specific contribution of parasite genetics (heritability) to this trait was only 5%. Our parasite source might possess minimal genetic diversity, which could explain its low heritability (and the high value of the vector). Notably, the environment contributed 28%. These estimates are relevant only to the particular system under study, but this experimental design could be useful for other parasite-host systems. The prospects and limitations of the genetic manipulation of vector populations to render the vector resistant to the parasite are better considered on the basis of this framework.

Show MeSH
Related in: MedlinePlus