Limits...
A virulent Wolbachia infection decreases the viability of the dengue vector Aedes aegypti during periods of embryonic quiescence.

McMeniman CJ, O'Neill SL - PLoS Negl Trop Dis (2010)

Bottom Line: Minor costs of wMelPop-CLA infection for pre-imaginal survivorship, development and adult size were found.These results reveal a general pattern associated with wMelPop-CLA induced pathogenesis in this mosquito species, where host fitness costs increase during aging of both immature and adult life-history stages.In addition to influencing the invasion dynamics of this particular Wolbachia strain, we suggest that the negative impact of wMelPop-CLA on embryonic quiescence may have applied utility as a tool to reduce mosquito population size in regions with pronounced dry seasons or in regions that experience cool winters.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, The University of Queensland, St Lucia, Queensland, Australia.

ABSTRACT
A new approach for dengue control has been proposed that relies on life-shortening strains of the obligate intracellular bacterium Wolbachia pipientis to modify mosquito population age structure and reduce pathogen transmission. Previously we reported the stable transinfection of the major dengue vector Aedes aegypti with a life-shortening Wolbachia strain (wMelPop-CLA) from the vinegar fly Drosophila melanogaster. Here, we report a further characterization of the phenotypic effects of this virulent Wolbachia infection on several life-history traits of Ae. aegypti. Minor costs of wMelPop-CLA infection for pre-imaginal survivorship, development and adult size were found. However, we discovered that the wMelPop-CLA infection dramatically decreased the viability of desiccated Ae. aegypti eggs over time. Similarly, the reproductive fitness of wMelPop-CLA infected Ae. aegypti females declined with age. These results reveal a general pattern associated with wMelPop-CLA induced pathogenesis in this mosquito species, where host fitness costs increase during aging of both immature and adult life-history stages. In addition to influencing the invasion dynamics of this particular Wolbachia strain, we suggest that the negative impact of wMelPop-CLA on embryonic quiescence may have applied utility as a tool to reduce mosquito population size in regions with pronounced dry seasons or in regions that experience cool winters.

Show MeSH

Related in: MedlinePlus

Age-associated decline in fecundity of PGYP1 and PGYP1.tet strains.(A) Average number of eggs oviposited per female ± SE. (B) Average number of larvae produced per female ± SE, and (C) Proportion of sampled females that did not oviposit. Females were assayed over successive gonotrophic cycles until death (n = 48 females per time-point). As death occurred over time, samples sizes decreased below 48 females in cycle 7 for PGYP1 females (n = 22), and in cycles 13–16 for PGYP1.tet females (n = 22, 12, 5, and 5 respectively).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2903475&req=5

pntd-0000748-g001: Age-associated decline in fecundity of PGYP1 and PGYP1.tet strains.(A) Average number of eggs oviposited per female ± SE. (B) Average number of larvae produced per female ± SE, and (C) Proportion of sampled females that did not oviposit. Females were assayed over successive gonotrophic cycles until death (n = 48 females per time-point). As death occurred over time, samples sizes decreased below 48 females in cycle 7 for PGYP1 females (n = 22), and in cycles 13–16 for PGYP1.tet females (n = 22, 12, 5, and 5 respectively).

Mentions: PGYP1 and PGYP1.tet females had similar reproductive outputs in terms of the number of eggs oviposited and the number of viable larvae hatched per female during their first gonotrophic cycle (Fig. 1A and B). However, during subsequent cycles both fecundity and fertility of PGYP1 females decreased at an accelerated rate (fecundity: R2 = 0.5068, F1,299 = 307.30, P<0.001; fertility: R2 = 0.3517, F1,299 = 162.20, P<0.001) relative to females from the PGYP1.tet strain (fecundity: R2 = 0.3167, F1,602 = 278.95, P<0.001; fertility: R2 = 0.1506, F1,602 = 106.76, P<0.001). For example, as PGYP1 females aged the average number of larvae produced per female decreased such that by the second cycle a 15% cost to reproductive output was observed relative to uninfected PGYP1.tet females, which progressively declined to a 40% cost by the fifth cycle (t-tests, P<0.05 for all comparisons). A large proportion of PGYP1 females that were randomly sampled for oviposition at the six and seventh gonotrophic cycles did not produce eggs (Fig. 1C), leading to a further decline in fecundity and fertility of this strain (Fig. 1A and B). This appeared to be due to defects in feeding behaviour, as many of these older PGYP1 females were observed to be unsuccessful in obtaining a blood meal (data not shown). Such a dramatic decrease in oviposition rates was not evident for PGYP1.tet females as they aged (Fig. 1C).


A virulent Wolbachia infection decreases the viability of the dengue vector Aedes aegypti during periods of embryonic quiescence.

McMeniman CJ, O'Neill SL - PLoS Negl Trop Dis (2010)

Age-associated decline in fecundity of PGYP1 and PGYP1.tet strains.(A) Average number of eggs oviposited per female ± SE. (B) Average number of larvae produced per female ± SE, and (C) Proportion of sampled females that did not oviposit. Females were assayed over successive gonotrophic cycles until death (n = 48 females per time-point). As death occurred over time, samples sizes decreased below 48 females in cycle 7 for PGYP1 females (n = 22), and in cycles 13–16 for PGYP1.tet females (n = 22, 12, 5, and 5 respectively).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2903475&req=5

pntd-0000748-g001: Age-associated decline in fecundity of PGYP1 and PGYP1.tet strains.(A) Average number of eggs oviposited per female ± SE. (B) Average number of larvae produced per female ± SE, and (C) Proportion of sampled females that did not oviposit. Females were assayed over successive gonotrophic cycles until death (n = 48 females per time-point). As death occurred over time, samples sizes decreased below 48 females in cycle 7 for PGYP1 females (n = 22), and in cycles 13–16 for PGYP1.tet females (n = 22, 12, 5, and 5 respectively).
Mentions: PGYP1 and PGYP1.tet females had similar reproductive outputs in terms of the number of eggs oviposited and the number of viable larvae hatched per female during their first gonotrophic cycle (Fig. 1A and B). However, during subsequent cycles both fecundity and fertility of PGYP1 females decreased at an accelerated rate (fecundity: R2 = 0.5068, F1,299 = 307.30, P<0.001; fertility: R2 = 0.3517, F1,299 = 162.20, P<0.001) relative to females from the PGYP1.tet strain (fecundity: R2 = 0.3167, F1,602 = 278.95, P<0.001; fertility: R2 = 0.1506, F1,602 = 106.76, P<0.001). For example, as PGYP1 females aged the average number of larvae produced per female decreased such that by the second cycle a 15% cost to reproductive output was observed relative to uninfected PGYP1.tet females, which progressively declined to a 40% cost by the fifth cycle (t-tests, P<0.05 for all comparisons). A large proportion of PGYP1 females that were randomly sampled for oviposition at the six and seventh gonotrophic cycles did not produce eggs (Fig. 1C), leading to a further decline in fecundity and fertility of this strain (Fig. 1A and B). This appeared to be due to defects in feeding behaviour, as many of these older PGYP1 females were observed to be unsuccessful in obtaining a blood meal (data not shown). Such a dramatic decrease in oviposition rates was not evident for PGYP1.tet females as they aged (Fig. 1C).

Bottom Line: Minor costs of wMelPop-CLA infection for pre-imaginal survivorship, development and adult size were found.These results reveal a general pattern associated with wMelPop-CLA induced pathogenesis in this mosquito species, where host fitness costs increase during aging of both immature and adult life-history stages.In addition to influencing the invasion dynamics of this particular Wolbachia strain, we suggest that the negative impact of wMelPop-CLA on embryonic quiescence may have applied utility as a tool to reduce mosquito population size in regions with pronounced dry seasons or in regions that experience cool winters.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, The University of Queensland, St Lucia, Queensland, Australia.

ABSTRACT
A new approach for dengue control has been proposed that relies on life-shortening strains of the obligate intracellular bacterium Wolbachia pipientis to modify mosquito population age structure and reduce pathogen transmission. Previously we reported the stable transinfection of the major dengue vector Aedes aegypti with a life-shortening Wolbachia strain (wMelPop-CLA) from the vinegar fly Drosophila melanogaster. Here, we report a further characterization of the phenotypic effects of this virulent Wolbachia infection on several life-history traits of Ae. aegypti. Minor costs of wMelPop-CLA infection for pre-imaginal survivorship, development and adult size were found. However, we discovered that the wMelPop-CLA infection dramatically decreased the viability of desiccated Ae. aegypti eggs over time. Similarly, the reproductive fitness of wMelPop-CLA infected Ae. aegypti females declined with age. These results reveal a general pattern associated with wMelPop-CLA induced pathogenesis in this mosquito species, where host fitness costs increase during aging of both immature and adult life-history stages. In addition to influencing the invasion dynamics of this particular Wolbachia strain, we suggest that the negative impact of wMelPop-CLA on embryonic quiescence may have applied utility as a tool to reduce mosquito population size in regions with pronounced dry seasons or in regions that experience cool winters.

Show MeSH
Related in: MedlinePlus