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Entomology in Focus 7
Walter R. Terra
Clelia Ferreira
Carlos P. Silva
Molecular
Physiology and
Evolution of Insect
Digestive Systems
Entomology in Focus
Volume 7
Insects are fundamentally important in the ecology of terrestrial habitats. What is
more, they affect diverse human activities, notably agriculture, as well as human
health and wellbeing. Meanwhile, much of modern biology has been developed
using insects as subjects of study.
To reflect this, our aim with Entomology in Focus is to offer a range of titles that
either capture different aspects of the diverse biology of insects or their management,
or that offer updates and reviews of particular species or taxonomic groups that are
important for agriculture, the environment or public health.
The series results from an agreement between Springer and the Entomological
Society of Brazil (SEB) and as such may lean towards tropical entomology. The aim
throughout is to provide reference texts that are simple in their conception and
organization but that offer up-to-date syntheses of the respective areas, offer
suggestions of future directions for research (and for management where relevant)
and that don’t shy away from offering considered opinions.
Editorial Committee
Series Editor Sam Elliot is Associate Professor in Entomology at the Universidade
Federal de Viçosa (Brazil), also coordinates the Postgraduate Programme in
Entomology currently rated maximally by the relevant authority in Brazil (CAPES)
and is Associate Editor at Ecology and Evolution. He works on diverse aspects of
insect-microbe interactions, with emphases on leafcutter ants, noctuid caterpillars,
triatomine bugs, entomopathogenic fungi and microbial control of pests.
Adam Hart is Professor of Science Communication at the University of
Gloucestershire (UK). His particular interest is in social insects but he has written
and broadcasted on a broad range of biological subjects. He presents documentaries
for BBC Radio 4, BBC4 and BBC2, as well as the weekly BBC radio programme
Science in Action.
Eugenio Oliveira is Assistant Professor in Entomology at the Universidade Federal
de Viçosa (Brazil), and scholar researcher of the Brazilian National Council of
Scientific and Technologic Development (CNPq). He has also working as Associate
Editor at the journals Neotropical Entomology and Invertebrate Neuroscience. He
works principally on insect neurophysiology, applying this in particular to
entomological/agricultural questions.
Ken Wilson is Professor of Evolutionary Ecology at Lancaster University (UK),
and is Executive Editor of the Journal of Animal Ecology. He is particularly
interested in host-parasite interactions and investigates these in invertebrate and
vertebrate hosts. Noctuid caterpillars, especially armyworms, have been one of his
main model systems and he is currently working on their ecology and biocontrol
in Africa.
Walter R. Terra • Clelia Ferreira • Carlos P. Silva
Molecular Physiology
and Evolution of Insect
Digestive Systems
Walter R. Terra Clelia Ferreira
Instituto de Química Instituto de Química
Universidade de São Paulo Universidade de São Paulo
São Paulo, Brazil São Paulo, Brazil
Carlos P. Silva
Departamento de Bioquímica
Universidade Federal de Santa Catarina
Florianópolis - SC, Brazil
© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature
Switzerland AG 2023
This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether
the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of
illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and
transmission or information storage and retrieval, electronic adaptation, computer software, or by similar
or dissimilar methodology now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication
does not imply, even in the absence of a specific statement, that such names are exempt from the relevant
protective laws and regulations and therefore free for general use.
The publisher, the authors, and the editors are safe to assume that the advice and information in this book
are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the
editors give a warranty, expressed or implied, with respect to the material contained herein or for any
errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional
claims in published maps and institutional affiliations.
This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
The whole field of insect midgut studies was covered in a book entitled Biology of
the Insect Midgut edited by M.J. Lehane and P.F. Billingsley in 1996 (Chapman &
Hall, London). Since then, highly efficient techniques of protein separation were
developed and a great amount of molecular manipulation procedures were intro-
duced or improved, like gene cloning and production of recombinant proteins, new-
generation sequencing methods, and techniques of suppression of protein expression.
The impact of the use of these methods on midgut studies was impressive, particu-
larly regarding the molecular mechanisms underlying digestion and absorption and
their evolution. These advances have been reviewed several times, but never in a
comprehensive book form.
The aim of this book is to provide a balanced blend of introductory and special-
ized aspects of the molecular mechanisms underlying insect midgut buffering,
digestion, nutrient absorption, and their changes along the evolution, ending with a
discussion on new technologies of insect control based on the information gathered
in the previous chapters.
The first part of the book (Chapters 1, 2, 3, and 4) comprises four major introduc-
tory subjects: the omics-based patterns of insect evolution, to be used to organize
the findings in an evolutionary perspective; overview of the methods and results
regarding the spatial organization of digestion and absorption; description of the
types and chemistry of insect diets; ordinary digestive enzymes that degrade dietary
molecules.
The second part of the book (Chaps. 5, 6, 7, and 8) describes the organization of
midgut cells, the function of their microvillar membranes and extracellular layers,
and, finally, their role in secretory processes. With this background, the function of
membrane transporters in the absorption of nutrients and maintenance of midgut pH
and water fluxes are detailed.
The third part of the book (Chaps. 8, 9, 10, 11, and 12) deals with special topics
like endocrine regulation of midgut function; adaptations to overcome the action of
digestive enzyme inhibitors; specializations to deal with plant, bacterial, and fungi
cell walls; and, finally, the role of microorganisms in nutrition.
vii
viii Preface
The last part of the book (Chaps. 13, 14, and 15) reviews the molecular mecha-
nisms underlying digestion and nutrient absorption in the major insect orders and
postulates how these processes changed along the evolution. The book ends with an
overview of the techniques of insect control that employs the knowledge gathered
along the midgut studies.
This book was written to be suitable for students and advanced scientists of ento-
mology, biology, biochemistry, genetics, pest control specialists, and for those
working with degradation of plant cell walls by insect or midgut microbial enzymes.
Work done in the laboratories of the authors was financed by the São Paulo Research
Foundation (FAPESP, Grant “Temático” no. 2017/08103-4), National Council of
Research (CNPq), and National Institute of Science and Technology-Molecular
Entomology (INCT-Entomologia Molecular).
1
Patterns of Insect Evolution�������������������������������������������������������������������� 1
1.1 Initial Considerations������������������������������������������������������������������������ 1
1.2 Polyneoptera ������������������������������������������������������������������������������������ 4
1.2.1 Dictyoptera���������������������������������������������������������������������������� 4
1.2.2 Orthoptera ���������������������������������������������������������������������������� 4
1.3 Condylognatha���������������������������������������������������������������������������������� 5
1.3.1 Thysanoptera������������������������������������������������������������������������ 5
1.3.2 Hemiptera������������������������������������������������������������������������������ 5
1.4 Holometabola������������������������������������������������������������������������������������ 6
1.4.1 Coleoptera ���������������������������������������������������������������������������� 6
1.4.2 Hymenoptera������������������������������������������������������������������������ 8
1.4.3 Diptera���������������������������������������������������������������������������������� 9
1.4.4 Lepidoptera �������������������������������������������������������������������������� 11
References�������������������������������������������������������������������������������������������������� 11
2
Overview of Insect Midgut Function������������������������������������������������������ 13
2.1 Food Handling and Ingestion������������������������������������������������������������ 14
2.2 Gut Morphology�������������������������������������������������������������������������������� 15
2.3 Stepwise Digestion of Nutrients ������������������������������������������������������ 18
2.4 Phases of Digestion and Their Compartmentalization in
the Midgut���������������������������������������������������������������������������������������� 20
2.5 Identification of the Sites of Transport of Water, Ions,
and Nutrients Along the Gut ������������������������������������������������������������ 24
References�������������������������������������������������������������������������������������������������� 25
3
Types and Chemistry of Diets ���������������������������������������������������������������� 27
3.1 Initial Considerations������������������������������������������������������������������������ 27
3.2 Detritus���������������������������������������������������������������������������������������������� 28
3.2.1 Types of Detritus������������������������������������������������������������������ 28
3.2.2 Litter Chemical Composition������������������������������������������������ 30
3.2.3 Litter and Wood Quality������������������������������������������������������� 33
ix
x Contents
Abstract Insects are the most diverse living beings and their ancestors moved from
the sea and colonized the land long before the chordates. Phylogenetic and fossil
data were combined to detail the patterns of insect evolution. Insects able to flex
their wings over the back (Neoptera) correspond to most of the insects and evolved
along the major lineages: Polyneoptera, Condylognatha, and Holometabola.
Polyneoptera includes Dictyoptera – cockroaches and termites that are omnivorous
or wood feeders and the carnivorous mantids – and Orthoptera – the omnivorous
crickets and grass-feeding grasshoppers. Condylognatha includes Hemiptera which
are the only insects able to live entirely on plant sap such as aphids, cicadas, and
spittlebugs; and others like bugs adapted to different diets. Holometabola is the
most successful lineage with 86% of the insect species, have complete metamor-
phosis (larva, pupa, and adult) and comprises the major insect orders: Coleoptera
(beetles); Hymenoptera (wasps, ants, and bees); Diptera (mosquitoes and flies); and
Lepidoptera (butterflies and moths). Insects of these orders explore the most diverse
food sources like other insects, stems, leaves and wood, seeds, keratin (like woolen
carpets), pollen, nectar, fungi, and vertebrate blood. The major selective pressures
affecting insect guts identified were: (a) adaptations to deal with large amounts of
dilute fluid food, (b) adaptations to digesting plant and fungal cells as a result of
horizontal transfer of genes from microorganisms and recruitment of lysosomal
proteins as digestive enzymes, (c) adaptations to avoiding plant inhibitors by gene
expansion and new functionalization, (d) and adaptations to avoiding prolonged
exposure to natural enemies and to living in short-lived media by reduction of life
span permitted by more efficient midguts.
1.1 Initial Considerations
This chapter overviews the patterns of insect evolution, highlighting the insect taxa
and specific insects that are more important for midgut studies.
Insects are the most diverse living beings and are found in practically all land
surfaces, except in the extreme polar regions and in the highest mountain peaks
(Daly et al. 1998). The success of the insects is measured by their large number of
species amounting to about half of the known living species and to almost 75% of
the animals. This success is supposed to rely on several of the insect’s characteris-
tics, such as its exoskeleton, flight capacity, small size, and ability to use diverse
nutritional sources.
The insect exoskeleton made of repetitive segments and appendages pre-adapted
them to walking on land, thus favoring their exit from the sea and the colonization
of terrestrial environments much earlier than the chordates. Flight permitted the
insects to escape from enemies and find mates, food, and sites to lay eggs. A small
size allowed the insects to live in small places and have short generation time
because less time is necessary to attain adulthood. Finally, the insect’s capacity to
rely on the most varied nutritional sources favors its adaptation to almost any envi-
ronment (Daly et al. 1998).
A list of the major insect orders with common names of the most known insects
is shown in Table 1.1.1. This table is expected to make it easier to follow the descrip-
tion of insect evolution. Non-winged insect ancestors, together with a few other
arthropods, were the first animals to invade the land, approximately at the same time
as plants in the Early Ordovician (circa 420 Ma) (Grimaldi and Engel 2005; Misof
et al. 2014). The most primitive insects were wingless (Infraclass Apterygotha) and
will not be considered here. The first winged insects (Infraclass Pterygotha) were
characterized by wings that cannot be flexed over the back at rest (Paleoptera) and
include Ephemeroptera (the mayflies) and the predatory Odonata (dragonflies and
damselflies). Neoptera corresponds to most insects, and they have wing flexing that
permits them to enter underneath environments like liter and bark.
Neoptera evolved along the major lineages Polyneoptera (Plecoptera, Orthoptera,
Phasmatodea, and Dictyoptera); Condylognatha (Thysanoptera and Hemiptera);
and a branch corresponding to Psocodea (Phthyraptera and Psocoptera) plus
Holometabola (Fig. 1.1). The once proposed clade Paraneoptera, comprising
Condylognatha and Psocodea, is paraphyletic because, as shown above,
Condylognatha is a sister group of Psocodea+Holometabola. Holometabola includes
Hymenoptera and a large grouping divided into two branches: Neuroptera+Coleoptera
and Panorpoidea. Panorpoidea is divided into two sister clades:
Trichoptera+Lepidoptera and Siphonaptera+Diptera (Fig. 1.1). The expansion of
Hymenoptera, Diptera, and Lepidoptera occurred in parallel with the radiation of
angiosperms in Early cretaceous (circa 100 Ma) (Misof et al. 2014).
Holometabola comprises 86%, Polyneoptera (mainly Orthoptera and Dyctioptera)
3.2%, and Condylognatha (mainly Hemiptera) 7.1% of the insect species. The evo-
lutionary success of Holometabola is supposed to result from the fact that their
young forms (larva) are adapted to ecological niches different from those of adults,
thus avoiding their competition for the same food, as occurs with insects without
complete metamorphosis (Polyneoptera, Condylognatha, and Psocodea). After this
overview of insect evolution, the major insect orders will be reviewed, calling
Fig. 1.1 Simplified phylogenetic tree of the relationships of the major insect orders. Number in
nodes mean: 1, Pterygotha; 2, Paleoptera; 3, Neoptera; 4, Polyneoptera; 5, Condylognatha; 6,
Psocodea; 7, Holometabola; 8, Panorpoidea. Geological periods: Devonian, Carboniferous,
Permian, Triassic, Jurassic, Cretaceous. (Details in text)
4 1 Patterns of Insect Evolution
attention to some remarkable species that are subject of studies of their digestive
systems and, finally, their internal phylogenetics will be discussed.
1.2 Polyneoptera
1.2.1 Dictyoptera
1.2.2 Orthoptera
Orthoptera are the dominant group of chewing hemimetabolous insects. The ances-
tors of Orthoptera gave rise to the crickets (suborder Ensifera, exemplified by
Gryllodes sigillatus), which are omnivorous or predatory, and the grasshoppers
(suborder Caelifera like Abracris flavolineata), which feed mainly on grasses.
Locusts are grasshoppers that periodically form large populations, attacking one
and then swarming to other places. Locusta migratoria, the migratory locust, is the
most widespread locust species being found mainly in all of Africa, Australia, and
New Zealand. Schistocerca gregaria, the desert locust, is found primarily in Africa,
Arabia, and West Asia. The phylogeny of Orthoptera is discussed by Zhang
et al. (2013).
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