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. 2020 Jan 7;13(1):4.
doi: 10.1186/s13071-020-3886-9.

Second generation effects of larval metal pollutant exposure on reproduction, longevity and insecticide tolerance in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

Alexander C S N Jeanrenaud  1   2 , Basil D Brooke  1   2 , Shüné V Oliver  3   4
Affiliations

Second generation effects of larval metal pollutant exposure on reproduction, longevity and insecticide tolerance in the major malaria vector Anopheles arabiensis (Diptera: Culicidae)

Alexander C S N Jeanrenaud et al. Parasit Vectors. .

Abstract

Background: Members of the Anopheles gambiae complex breed in clean, sunlit temporary bodies of water. Anthropogenic pollution is, however, altering the breeding sites of the vectors with numerous biological effects. Although the effects of larval metal pollution have previously been examined, this study aims to assess the transgenerational effects of larval metal pollution on the major malaria vector An. arabiensis.

Methods: Two laboratory strains of An. arabiensis, SENN (insecticide-susceptible) and SENN-DDT (insecticide-resistant), were used in this study. After being bred in water polluted with either cadmium chloride, copper nitrate or lead nitrate, several life history characteristics that can have epidemiological implications (fertility, apoptotic damage to reproductive structures, adult longevity and insecticide tolerance) were examined in the adults and compared to those of adults bred in clean water.

Results: All metal treatments reduced fecundity in SENN, but only lead treatment reduced fertility in SENN-DDT. Cadmium chloride exposure resulted in apoptosis and deformation of the testes in both strains. After breeding generation F0 in polluted water, F1 larvae bred in clean water showed an increase in longevity in SENN-DDT adult females. In contrast, after breeding the F0 generation in polluted water, longevity was reduced after cadmium and copper exposure in the F1 generation. Larval metal exposure resulted in an increase in insecticide tolerance in adults of the SENN strain, with SENN-DDT adults gaining the greatest fold increase in insecticide tolerance.

Conclusions: This study demonstrates that a single exposure to metal pollution can have transgenerational effects that are not negated by subsequent breeding in clean water.

Keywords: Anopheles arabiensis; Insecticide resistance; Longevity; Transgenerational effects.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Schema of the mating experiments to determine whether male or female larval heavy metal treatment affects fertility or fecundity
Fig. 2
Fig. 2
The effect of heavy metal exposure on the fertility and fecundity of Anopheles arabiensis. a The total number of eggs laid by SENN and SENN-DDT, where C represents control and T represents the respective metal treatment. b The average number of eggs laid per female by SENN and SENN-DDT, where C represents control and T represents the respective metal treatment. c Average hatch percentage off eggs laid by SENN and SENN-DDT. Asterisks indicate a significant difference from the control
Fig. 3
Fig. 3
The effect of larval heavy metal exposure on apoptosis levels in the testes and eggs of Anopheles arabiensis. a The effect of larval exposure to metals on levels of apoptosis (indicated by red staining) in adult SENN (A-D) and SENN-DDT (G-H). b The effects of larval exposure to metals on oviposited eggs from SENN (A-D) and SENN-DDT (G-H)
Fig. 4
Fig. 4
The effect of larval heavy metal exposure on parental (F0) and second-generation (F1) adult longevity in Anopheles arabiensis. a The effect of larval cadmium chloride exposure on a parental generation and second-generation (SENNConF- Control female, SENNConM-Control male, SENNCdFC-female cadmium second-generation from clean water, SENNCdMC-male cadmium second-generation from clean water, SENNCdFP- female cadmium second-generation from polluted water, SENNCdMP- male cadmium second-generation from polluted water) for the SENN strain. b The effect of copper nitrate exposure on a parental generation and second-generation for the SENN strain. c The effect of lead nitrate exposure on a parental generation and second-generation for the SENN strain. d The effect of cadmium chloride exposure on a parental generation and second-generation for the SENN-DDT strain. e The effect of copper nitrate exposure on a parental generation and second-generation for the SENN-DDT strain. f The effect of lead nitrate exposure on a parental generation and second-generation for the SENN-DDT strain
Fig. 5
Fig. 5
The transgenerational effects of larval metal pollutant exposure on insecticide tolerance in adult Anopheles arabiensis. a The effect of larval metal pollution on the deltamethrin (Delta) and malathion (Mal)-induced lethal times to 50% mortality (LT50) for the insecticide-susceptible SENN strain. The control, deltamethrin and malathion LT50s were determined from standard 3-day-old SENN non-blood-fed adults. This is compared to first generation metal exposed (F0) as well as second-generation adults reared from larvae bred in clean water (F1C) and second-generation adults reared from larvae exposed to the same pollutant as the parental generation (F1P). Asterisks indicate a significant difference in LT50 from the lethal time of the adults reared in clean water (control). b The effect of larval metal pollution on the deltamethrin (Delta) and malathion (Mal)-induced LT50s for the insecticide-resistant SENN-DDT strain. The control deltamethrin and malathion LT50s were determined from standard 3-day-old SENN non-blood-fed adults
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