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

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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Cell and Tissue Research (2023) 393:297–320
https://doi.org/10.1007/s00441-023-03783-5
REGULAR ARTICLE
The larval midgut ofAnopheles, Aedes, andToxorhynchites mosquitoes
(Diptera, Culicidae): acomparative approach inmorphophysiology
andevolution
RaquelSoaresMaiaGodoy1,4 · RenataCristinaBarbosa1· WeiHuang2· NágilaFrancineteCostaSecundino3·
PauloFilemonPaolucciPimenta3· MarceloJacobs‑Lorena2· GustavoFerreiraMartins1
Received: 5 May 2022 / Accepted: 8 May 2023 / Published online: 5 June 2023
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023
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 (gas-
tric 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.
Keywords Digestive tract· Histology· Histochemistry· Gastric caecum· Enterocytes· Enteroendocrine cells
Introduction
Culicidae (Insecta, Diptera) is a large and diverse mono-
phyletic group of insects known as mosquitoes. They are
mainly found in the tropical and subtropical regions of the
globe but are also in temperate regions, and even in polar
zones. There are around 3583 species registered, which are
classified into two subfamilies (Anophelinae and Culicinae)
and 113 genera (https:// mosqu ito- taxon omic- inven tory. info/
accessed on 12 May 21). Most adult female mosquitoes are
blood feeders. This characteristic is responsible for the medi-
cal importance of the group, as it enables transmission of
many pathogens such as arboviruses (Rodrigues etal. 2021),
Plasmodium protozoans (Pimenta etal. 1994, Molina-Cruz
etal.2016), and filarial worms (Michalski etal.2010) to the
vertebrate host. On the other hand, females of some species,
such as those belonging to the Toxorhynchites genus, and all
adult male mosquitoes, are exclusively sugar feeders (Godoy
etal. 2015; Donald etal. 2020).
Mosquitoes are holometabolic insects and undergo a
developmental process that includes the immature stages of
larvae and pupae (both aquatic) before the emergence of
the adults (terrestrial) (Rolff etal. 2019). Adult mosquitoes
are morphologically extremely distinct from larvae. They
* Raquel Soares Maia Godoy
quel_maia1@hotmail.com
1 Departamento de Biologia Geral, Universidade Federal de
Viçosa, Viçosa,MinasGerais36570-900, Brazil
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
3 Fundação Oswaldo Cruz, Instituto René Rachou, Fiocruz,
30190-002, BeloHorizonte, MinasGerais, Brazil
4 Current affiliation: Fundação Oswaldo Cruz, Instituto René
Rachou, Fiocruz, BeloHorizonte, MinasGerais30190-002,
Brazil
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