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The larval midgut of Anopheles, Aedes, and Toxorhynchites mosquitoes (Diptera, Culicidae): a comparative approach in morphophysiology and evolution

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Abstract

The mosquito larval midgut is responsible for acquiring and storing most of the nutrients that will sustain the events of metamorphosis and the insect’s adult life. Despite its importance, the basic biology of this larval organ is poorly understood. To help fill this gap, we carried out a comparative morphophysiological investigation of three larval midgut regions (gastric caeca, anterior midgut, and posterior midgut) of phylogenetically distant mosquitoes: Anopheles gambiae (Anopheles albimanus was occasionally used as an alternate), Aedes aegypti, and Toxorhynchites theobaldi. Larvae of Toxorhynchites mosquitoes are predacious, in contrast to the other two species, that are detritivorous. In this work, we show that the larval gut of the three species shares basic histological characteristics, but differ in other aspects. The lipid and carbohydrate metabolism of the An. gambiae larval midgut is different compared with that of Ae. aegypti and Tx. theobaldi. The gastric caecum is the most variable region, with differences probably related to the chemical composition of the diet. The peritrophic matrix is morphologically similar in the three species, and processes involved in the post-embryonic development of the organ, such as cell differentiation and proliferation, were also similar. FMRF-positive enteroendocrine cells are grouped in the posterior midgut of Tx. theobaldi, but individualized in An. gambiae and Ae. aegypti. We hypothesize that Tx. theobaldi larval predation is an ancestral condition in mosquito evolution.

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Acknowledgements

To the Núcleo de Microscopia e Microanálise (NMM, UFV) and the Program for Technological Development in Tools for Health-PDTIS-FIOCRUZ for technical assistance.

Funding

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, 001)—support to RSMG; Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig; APQ-00560–17) and Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brasil (CNPq—301725/2019–5)—support to GFM; Instituto Nacional de Ciência e Tecnologia—Entomologia Molecular (INCT-EM)—support to NFCS; CAPES—support to PFPP; National Institutes of Health (USA) R01AI031478 and the Bloomberg Philanthropies—support to MJL.

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Authors and Affiliations

  1. Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Raquel Soares Maia Godoy, Renata Cristina Barbosa & Gustavo Ferreira Martins

  2. The W. Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Malaria Research Institute, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, 21205, USA

    Wei Huang & Marcelo Jacobs-Lorena

  3. Fundação Oswaldo Cruz, Instituto René Rachou, Fiocruz, 30190-002, Belo Horizonte, Minas Gerais, Brazil

    Nágila Francinete Costa Secundino & Paulo Filemon Paolucci Pimenta

  4. Current affiliation: Fundação Oswaldo Cruz, Instituto René Rachou, Fiocruz, Belo Horizonte, Minas Gerais, 30190-002, Brazil

    Raquel Soares Maia Godoy

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Godoy, R.S.M., Barbosa, R.C., Huang, W. et al. The larval midgut of Anopheles, Aedes, and Toxorhynchites mosquitoes (Diptera, Culicidae): a comparative approach in morphophysiology and evolution. Cell Tissue Res 393, 297–320 (2023). https://doi.org/10.1007/s00441-023-03783-5

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