Carryover effects of larval exposure to different environmental bacteria drive adult trait variation in a mosquito vector

Dickson, Laura B.; Jiolle, Davy; Minard, Guillaume; Moltini-Conclois, Isabelle; Volant, Stevenn; Ghozlane, Amine; Bouchier, Christiane; Ayala, Diégo; Paupy, Christophe; Moro, Claire Valiente; Lambrechts, Louis

doi:10.1126/sciadv.1700585

Cited by 174 publications

(271 citation statements)

References 70 publications

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“…First, experimental studies show that mosquito larvae hatch with no extracellular microbes in their gut [13]. Second, studies of gut community composition indicate that most microbes identified in larvae overlap with the community of microbes that are present in their aquatic habitat [13–18]. Third, mosquitoes host highly variable gut communities [13–18], which would not be expected if these communities were acquired directly from parents or congeners.…”

Section: Acquisition Of a Gut Microbiota By Mosquito Larvaementioning

confidence: 99%

“…Second, studies of gut community composition indicate that most microbes identified in larvae overlap with the community of microbes that are present in their aquatic habitat [13–18]. Third, mosquitoes host highly variable gut communities [13–18], which would not be expected if these communities were acquired directly from parents or congeners. Exceptions to environmental acquisition are results showing that several types of bacteria are present in the reproductive tracts of adult mosquitoes, and that some of these bacteria are on the surface of eggs females lay [13, 15, 19–25].…”

Section: Acquisition Of a Gut Microbiota By Mosquito Larvaementioning

confidence: 99%

“…Bacteria in these phyla are also common community members in insects from several other orders that acquire their gut microbiota from the environment [49], which suggests prevalence in part reflects their abundance in habitats insects frequent. Several bacteria identified as gut community members in mosquitoes have also been isolated and successfully cultured [13, 18, 22, 31, 50–53]. Unicellular eukaryotes identified as gut community members in different species of mosquitoes include fungi, algae, and Apicomplexa but thus far none of these organisms have been isolated from mosquitoes and cultured independently [43, 48, 54–57].…”

Section: Composition Of the Gut Microbiotamentioning

confidence: 99%

“…Studies of Aedes aegypti further show that substantial numbers of bacteria in the gut die at the end of each instar prior to molting, which provides opportunity for altering gut community composition in the succeeding instar [61]. Other patterns of note include that bacterial species diversity is consistently higher in mosquito larvae than adults [13, 15, 18, 47], and that diversity is lower in laboratory reared versus field collected mosquitoes of the same species [13, 14, 35]. …”

Section: Composition Of the Gut Microbiotamentioning

confidence: 99%

“…A large number of studies indicate that bacterial diversity differs substantially both between and within mosquito species as a function of collection location and other factors [14–18, 30, 42–46, 62, 63]. On a local scale, factors implicated in affecting community composition include habitat preferences of different mosquito species and larval feeding behavior [18, 30, 62].…”

Section: Composition Of the Gut Microbiotamentioning

confidence: 99%

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Composition and functional roles of the gut microbiota in mosquitoes

Strand

2018

Current Opinion in Insect Science

103

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An estimated 3500 species of mosquitoes (family Culicidae) exist worldwide of which several are known vectors of pathogens that cause disease in humans and other vertebrates. Mosquitoes also host communities of microbes in their digestive tract that form a gut microbiota. Recent studies provide important insights on how mosquitoes acquire a gut microbiota and the community of microbes that are present. Results also indicate that the gut microbiota affects several aspects of mosquito biology. Altogether, these effects impact mosquito fitness with potential consequences for disease prevalence.

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Section: Acquisition Of a Gut Microbiota By Mosquito Larvaementioning

confidence: 99%

Section: Acquisition Of a Gut Microbiota By Mosquito Larvaementioning

confidence: 99%

Section: Composition Of the Gut Microbiotamentioning

confidence: 99%

Section: Composition Of the Gut Microbiotamentioning

confidence: 99%

Section: Composition Of the Gut Microbiotamentioning

confidence: 99%

See 3 more Smart Citations

Composition and functional roles of the gut microbiota in mosquitoes

Strand

2018

Current Opinion in Insect Science

103

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Transstadial immune activation in a mosquito: Adults that emerge from infected larvae have stronger antibacterial activity in their hemocoel yet increased susceptibility to malaria infection

Brown

Shapiro

Thompson

et al. 2019

Ecology and Evolution

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Larval and adult mosquitoes mount immune responses against pathogens that invade their hemocoel. Although it has been suggested that a correlation exists between immune processes across insect life stages, the influence that an infection in the hemocoel of a larva has on the immune system of the eclosed adult remains unknown. Here, we used Anopheles gambiae to test whether a larval infection influences the adult response to a subsequent bacterial or malaria parasite infection. We found that for both female and male mosquitoes, a larval infection enhances the efficiency of bacterial clearance following a secondary infection in the hemocoel of adults. The adults that emerge from infected larvae have more hemocytes than adults that emerge from naive or injured larvae, and individual hemocytes have greater phagocytic activity. Furthermore, mRNA abundance of immune genes—such as cecropin A, Lysozyme C1, Stat‐A, and Tep1—is higher in adults that emerge from infected larvae. A larval infection, however, does not have a meaningful effect on the probability that female adults will survive a systemic bacterial infection, and increases the susceptibility of females to Plasmodium yoelii, as measured by oocyst prevalence and intensity in the midgut. Finally, immune proficiency varies by sex; females exhibit increased bacterial killing, have twice as many hemocytes, and more highly express immune genes. Together, these results show that a larval hemocoelic infection induces transstadial immune activation—possibly via transstadial immune priming—but that it confers both costs and benefits to the emerged adults.

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Larval sites of the mosquito Aedes aegypti formosus in forest and domestic habitats in Africa and the potential association with oviposition evolution

Xia

Dweck

Lutomiah

et al. 2021

Ecology and Evolution

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Adaptations to anthropogenic domestic habitats contribute to the success of the mosquito Aedes aegypti as a major global vector of several arboviral diseases. The species inhabited African forests before expanding into domestic habitats and spreading to other continents. Despite a well-studied evolutionary history, how this species initially moved into human settlements in Africa remains unclear. During this initial habitat transition, African Ae. aegypti switched their larval sites from natural water containers like tree holes to artificial containers like clay pots. Little is known about how these natural versus artificial containers differ in their characteristics.Filling this knowledge gap could provide valuable information for studying the evolution of Ae. aegypti associated with larval habitat changes. As an initial effort, in this study, we characterized the microenvironments of Ae. aegypti larval sites in forest and domestic habitats in two African localities: La Lopé, Gabon, and Rabai, Kenya. Specifically, we measured the physical characteristics, microbial density, bacterial composition, and volatile chemical profiles of multiple larval sites. In both localities, comparisons between natural containers in the forests and artificial containers in the villages revealed significantly different microenvironments. We next examined whether the between-habitat differences in larval site microenvironments lead to differences in oviposition, a key behavior affecting larval distribution. Forest Ae. aegypti readily accepted the artificial containers we placed in the forests. Laboratory choice experiments also did not find distinct oviposition preferences between forest and village Ae. aegypti colonies. These results suggested that African Ae. aegypti are likely generalists in their larval site choices. This flexibility to accept various containers with a wide range of physical, microbial, and chemical conditions might allow Ae. aegypti to use human-stored water as fallback larval sites during dry seasons, which is hypothesized to have initiated the domestic evolution of Ae. aegypti.

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Carryover effects of larval exposure to different environmental bacteria drive adult trait variation in a mosquito vector

Abstract: The adult phenotype of mosquitoes depends on the types of bacteria encountered environmentally during development.

Cited by 174 publications

References 70 publications

Composition and functional roles of the gut microbiota in mosquitoes

Composition and functional roles of the gut microbiota in mosquitoes

Transstadial immune activation in a mosquito: Adults that emerge from infected larvae have stronger antibacterial activity in their hemocoel yet increased susceptibility to malaria infection

Larval sites of the mosquito Aedes aegypti formosus in forest and domestic habitats in Africa and the potential association with oviposition evolution

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