Host–plant relations of gall-inducing insects

Donald Miller, Anantanarayanan Raman

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Abstract

Galls are modified, invariably symmetrical, naturally developing plant structures that arise because of messages from certain specialist insects, mostly from the Thysanoptera, Hemiptera, Diptera, and Hymenoptera, and in a lesser frequency from the Lepidoptera and Coleoptera. Several species of the Eriophyoidea (Acari) induce galls and wherever appropriate, we have considered examples from the Eriophyoidea as well, generically referred under the term“insects”.The insects live within them, deriving nourishment and shelter.When these insects attack plant tissues, osmotic-change–related stress increases, thus stimulating alterations in gas exchange and subcellular metabolic functions. The osmotic stress alters the electrical properties of the plant-cell plasma membranes and impacts on indole-acetic acid synthesis and activity, which, in turn, affects the H + -transport. Insect action stimulates parts of host-cell wall to break down and the degenerated wall materials in the cytoplasm act as elicitors. In such contexts the susceptible plants use flexible strategies to mitigate stress, which generally manifest as galls. Inherited traits also play a role in providing specific shapes to the gall, which is coordinated by the innate correlating morphogenetic factors that operate normally in the plant.The gall-inducing Diptera (Cecidomyiidae), Hemiptera (Sternorrhyncha), and Hymenoptera (Cynipidae) induce galls of highly defined and exquisite shapes. Almost all of these insects are known for their specificity to plants.The gall-inducing insects, unlike many of their free-living relatives, discriminate between plants and choose from them. Selection of a particular plant by a gall-inducing insect is not a matter of chance, given that the insect encounters varied plant taxa in the natural environment. The gall-inducing insects preferentially feed on specific plant organs, or parts of these, and on specific plant species. One recent explanation is that the gall-inducing insects prefer certain plants or parts of those plants, because they need the lipidic materials, e.g., sterols, available in those plant parts, which the insects utilize for building hormones critically necessary for their metamorphosis. Because of the sedentary nature of the juvenile stages of the inducing insect, the gravid females endowed with specialized sensory structures play a key role in selecting the site precisely for oviposition and thus for the progeny. Although a majority of gall-inducing insects are restricted to specific plant taxa, some of them, as we presently know, are indicated to be capable of inducing galls on plant species closely related to their most-preferred hosts, thus demonstrating some level of oligophagy. A few species of Asphondyliina and Schizomyiina (Cecidomyiidae) are presently indicated as polyphagous. Clearly demonstrated host shifts and adaptive radiation in some of the European and North-American gall-inducingTephritidae populations explain the evolution of sympatric host races, more because of changes either in the preference of feeding and/or oviposition sites or by acquiring “new” physiological adaptations to new plants or through assortative mating. Differences in the temporally regulated flowering and leafing phenologies in the susceptible plants possibly play a role in isolating gall-inducing insect populations, which enable divergence and diversification via genetic drift.The general understanding, as of now, is that host shifts and radiation in gall-inducing insects are more complex than what is known in their non-gall-inducing allies. Such a complexity is attributed to intricate relationships of gall-inducing insects with plants and the dispersal of gall-inducing insects through different biogeographical realms, mainly influenced by the abundance and variety of plant species.The gall-inducing insects, as a highly evolved group, present a stunning diversity, yet share the distinct capacity to redirect developmental programs of plants by generating galls. Propagation of the progeny manifests more prominently in the hemipteroids and Acari, whereas this behavior is not that prominent in the more-derived gall-inducing groups, such as the Cecidomyiidae and Cynipidae, wherein the gall as a facility is better used for the nutrition and development of the immature stages of the inducing insect taxon. The gall-inducing insects are easy to monitor because of the distinct presence of galls, offering an advantage in extending in investigations about the eco-physiology of several other economically important, non-gall-inducing insects.The gall-inducing insects could be termed as ecosystem engineers in the sense that they manipulate plant architecture to create novel habitats. Their impacts on plants will continue to bear scrutiny, especially in regions where gall-inducing insects have been introduced and released from their natural enemies, thus potently threatening various other plants, including the economically relevant ones. © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved.
Original languageEnglish
Pages (from-to)1-19
Number of pages19
JournalAnnals of the Entomological Society of America
Volume112
Issue number1
Early online dateOct 2018
DOIs
Publication statusPublished - Jan 2019

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galls
insects
Cecidomyiidae
gall-inducing insects
plant anatomy
Cynipidae
oviposition sites
osmotic stress
Acari
Hemiptera
Hymenoptera
Sternorrhyncha
electrical properties
assortative mating
adaptive radiation
ecophysiology
gravid females
feeding preferences
plant architecture
plant organs

Cite this

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title = "Host–plant relations of gall-inducing insects",
abstract = "Galls are modified, invariably symmetrical, naturally developing plant structures that arise because of messages from certain specialist insects, mostly from the Thysanoptera, Hemiptera, Diptera, and Hymenoptera, and in a lesser frequency from the Lepidoptera and Coleoptera. Several species of the Eriophyoidea (Acari) induce galls and wherever appropriate, we have considered examples from the Eriophyoidea as well, generically referred under the term“insects”.The insects live within them, deriving nourishment and shelter.When these insects attack plant tissues, osmotic-change–related stress increases, thus stimulating alterations in gas exchange and subcellular metabolic functions. The osmotic stress alters the electrical properties of the plant-cell plasma membranes and impacts on indole-acetic acid synthesis and activity, which, in turn, affects the H + -transport. Insect action stimulates parts of host-cell wall to break down and the degenerated wall materials in the cytoplasm act as elicitors. In such contexts the susceptible plants use flexible strategies to mitigate stress, which generally manifest as galls. Inherited traits also play a role in providing specific shapes to the gall, which is coordinated by the innate correlating morphogenetic factors that operate normally in the plant.The gall-inducing Diptera (Cecidomyiidae), Hemiptera (Sternorrhyncha), and Hymenoptera (Cynipidae) induce galls of highly defined and exquisite shapes. Almost all of these insects are known for their specificity to plants.The gall-inducing insects, unlike many of their free-living relatives, discriminate between plants and choose from them. Selection of a particular plant by a gall-inducing insect is not a matter of chance, given that the insect encounters varied plant taxa in the natural environment. The gall-inducing insects preferentially feed on specific plant organs, or parts of these, and on specific plant species. One recent explanation is that the gall-inducing insects prefer certain plants or parts of those plants, because they need the lipidic materials, e.g., sterols, available in those plant parts, which the insects utilize for building hormones critically necessary for their metamorphosis. Because of the sedentary nature of the juvenile stages of the inducing insect, the gravid females endowed with specialized sensory structures play a key role in selecting the site precisely for oviposition and thus for the progeny. Although a majority of gall-inducing insects are restricted to specific plant taxa, some of them, as we presently know, are indicated to be capable of inducing galls on plant species closely related to their most-preferred hosts, thus demonstrating some level of oligophagy. A few species of Asphondyliina and Schizomyiina (Cecidomyiidae) are presently indicated as polyphagous. Clearly demonstrated host shifts and adaptive radiation in some of the European and North-American gall-inducingTephritidae populations explain the evolution of sympatric host races, more because of changes either in the preference of feeding and/or oviposition sites or by acquiring “new” physiological adaptations to new plants or through assortative mating. Differences in the temporally regulated flowering and leafing phenologies in the susceptible plants possibly play a role in isolating gall-inducing insect populations, which enable divergence and diversification via genetic drift.The general understanding, as of now, is that host shifts and radiation in gall-inducing insects are more complex than what is known in their non-gall-inducing allies. Such a complexity is attributed to intricate relationships of gall-inducing insects with plants and the dispersal of gall-inducing insects through different biogeographical realms, mainly influenced by the abundance and variety of plant species.The gall-inducing insects, as a highly evolved group, present a stunning diversity, yet share the distinct capacity to redirect developmental programs of plants by generating galls. Propagation of the progeny manifests more prominently in the hemipteroids and Acari, whereas this behavior is not that prominent in the more-derived gall-inducing groups, such as the Cecidomyiidae and Cynipidae, wherein the gall as a facility is better used for the nutrition and development of the immature stages of the inducing insect taxon. The gall-inducing insects are easy to monitor because of the distinct presence of galls, offering an advantage in extending in investigations about the eco-physiology of several other economically important, non-gall-inducing insects.The gall-inducing insects could be termed as ecosystem engineers in the sense that they manipulate plant architecture to create novel habitats. Their impacts on plants will continue to bear scrutiny, especially in regions where gall-inducing insects have been introduced and released from their natural enemies, thus potently threatening various other plants, including the economically relevant ones. {\circledC} The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved.",
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Host–plant relations of gall-inducing insects. / Miller, Donald; Raman, Anantanarayanan.

In: Annals of the Entomological Society of America, Vol. 112, No. 1, 01.2019, p. 1-19.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Host–plant relations of gall-inducing insects

AU - Miller, Donald

AU - Raman, Anantanarayanan

PY - 2019/1

Y1 - 2019/1

N2 - Galls are modified, invariably symmetrical, naturally developing plant structures that arise because of messages from certain specialist insects, mostly from the Thysanoptera, Hemiptera, Diptera, and Hymenoptera, and in a lesser frequency from the Lepidoptera and Coleoptera. Several species of the Eriophyoidea (Acari) induce galls and wherever appropriate, we have considered examples from the Eriophyoidea as well, generically referred under the term“insects”.The insects live within them, deriving nourishment and shelter.When these insects attack plant tissues, osmotic-change–related stress increases, thus stimulating alterations in gas exchange and subcellular metabolic functions. The osmotic stress alters the electrical properties of the plant-cell plasma membranes and impacts on indole-acetic acid synthesis and activity, which, in turn, affects the H + -transport. Insect action stimulates parts of host-cell wall to break down and the degenerated wall materials in the cytoplasm act as elicitors. In such contexts the susceptible plants use flexible strategies to mitigate stress, which generally manifest as galls. Inherited traits also play a role in providing specific shapes to the gall, which is coordinated by the innate correlating morphogenetic factors that operate normally in the plant.The gall-inducing Diptera (Cecidomyiidae), Hemiptera (Sternorrhyncha), and Hymenoptera (Cynipidae) induce galls of highly defined and exquisite shapes. Almost all of these insects are known for their specificity to plants.The gall-inducing insects, unlike many of their free-living relatives, discriminate between plants and choose from them. Selection of a particular plant by a gall-inducing insect is not a matter of chance, given that the insect encounters varied plant taxa in the natural environment. The gall-inducing insects preferentially feed on specific plant organs, or parts of these, and on specific plant species. One recent explanation is that the gall-inducing insects prefer certain plants or parts of those plants, because they need the lipidic materials, e.g., sterols, available in those plant parts, which the insects utilize for building hormones critically necessary for their metamorphosis. Because of the sedentary nature of the juvenile stages of the inducing insect, the gravid females endowed with specialized sensory structures play a key role in selecting the site precisely for oviposition and thus for the progeny. Although a majority of gall-inducing insects are restricted to specific plant taxa, some of them, as we presently know, are indicated to be capable of inducing galls on plant species closely related to their most-preferred hosts, thus demonstrating some level of oligophagy. A few species of Asphondyliina and Schizomyiina (Cecidomyiidae) are presently indicated as polyphagous. Clearly demonstrated host shifts and adaptive radiation in some of the European and North-American gall-inducingTephritidae populations explain the evolution of sympatric host races, more because of changes either in the preference of feeding and/or oviposition sites or by acquiring “new” physiological adaptations to new plants or through assortative mating. Differences in the temporally regulated flowering and leafing phenologies in the susceptible plants possibly play a role in isolating gall-inducing insect populations, which enable divergence and diversification via genetic drift.The general understanding, as of now, is that host shifts and radiation in gall-inducing insects are more complex than what is known in their non-gall-inducing allies. Such a complexity is attributed to intricate relationships of gall-inducing insects with plants and the dispersal of gall-inducing insects through different biogeographical realms, mainly influenced by the abundance and variety of plant species.The gall-inducing insects, as a highly evolved group, present a stunning diversity, yet share the distinct capacity to redirect developmental programs of plants by generating galls. Propagation of the progeny manifests more prominently in the hemipteroids and Acari, whereas this behavior is not that prominent in the more-derived gall-inducing groups, such as the Cecidomyiidae and Cynipidae, wherein the gall as a facility is better used for the nutrition and development of the immature stages of the inducing insect taxon. The gall-inducing insects are easy to monitor because of the distinct presence of galls, offering an advantage in extending in investigations about the eco-physiology of several other economically important, non-gall-inducing insects.The gall-inducing insects could be termed as ecosystem engineers in the sense that they manipulate plant architecture to create novel habitats. Their impacts on plants will continue to bear scrutiny, especially in regions where gall-inducing insects have been introduced and released from their natural enemies, thus potently threatening various other plants, including the economically relevant ones. © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved.

AB - Galls are modified, invariably symmetrical, naturally developing plant structures that arise because of messages from certain specialist insects, mostly from the Thysanoptera, Hemiptera, Diptera, and Hymenoptera, and in a lesser frequency from the Lepidoptera and Coleoptera. Several species of the Eriophyoidea (Acari) induce galls and wherever appropriate, we have considered examples from the Eriophyoidea as well, generically referred under the term“insects”.The insects live within them, deriving nourishment and shelter.When these insects attack plant tissues, osmotic-change–related stress increases, thus stimulating alterations in gas exchange and subcellular metabolic functions. The osmotic stress alters the electrical properties of the plant-cell plasma membranes and impacts on indole-acetic acid synthesis and activity, which, in turn, affects the H + -transport. Insect action stimulates parts of host-cell wall to break down and the degenerated wall materials in the cytoplasm act as elicitors. In such contexts the susceptible plants use flexible strategies to mitigate stress, which generally manifest as galls. Inherited traits also play a role in providing specific shapes to the gall, which is coordinated by the innate correlating morphogenetic factors that operate normally in the plant.The gall-inducing Diptera (Cecidomyiidae), Hemiptera (Sternorrhyncha), and Hymenoptera (Cynipidae) induce galls of highly defined and exquisite shapes. Almost all of these insects are known for their specificity to plants.The gall-inducing insects, unlike many of their free-living relatives, discriminate between plants and choose from them. Selection of a particular plant by a gall-inducing insect is not a matter of chance, given that the insect encounters varied plant taxa in the natural environment. The gall-inducing insects preferentially feed on specific plant organs, or parts of these, and on specific plant species. One recent explanation is that the gall-inducing insects prefer certain plants or parts of those plants, because they need the lipidic materials, e.g., sterols, available in those plant parts, which the insects utilize for building hormones critically necessary for their metamorphosis. Because of the sedentary nature of the juvenile stages of the inducing insect, the gravid females endowed with specialized sensory structures play a key role in selecting the site precisely for oviposition and thus for the progeny. Although a majority of gall-inducing insects are restricted to specific plant taxa, some of them, as we presently know, are indicated to be capable of inducing galls on plant species closely related to their most-preferred hosts, thus demonstrating some level of oligophagy. A few species of Asphondyliina and Schizomyiina (Cecidomyiidae) are presently indicated as polyphagous. Clearly demonstrated host shifts and adaptive radiation in some of the European and North-American gall-inducingTephritidae populations explain the evolution of sympatric host races, more because of changes either in the preference of feeding and/or oviposition sites or by acquiring “new” physiological adaptations to new plants or through assortative mating. Differences in the temporally regulated flowering and leafing phenologies in the susceptible plants possibly play a role in isolating gall-inducing insect populations, which enable divergence and diversification via genetic drift.The general understanding, as of now, is that host shifts and radiation in gall-inducing insects are more complex than what is known in their non-gall-inducing allies. Such a complexity is attributed to intricate relationships of gall-inducing insects with plants and the dispersal of gall-inducing insects through different biogeographical realms, mainly influenced by the abundance and variety of plant species.The gall-inducing insects, as a highly evolved group, present a stunning diversity, yet share the distinct capacity to redirect developmental programs of plants by generating galls. Propagation of the progeny manifests more prominently in the hemipteroids and Acari, whereas this behavior is not that prominent in the more-derived gall-inducing groups, such as the Cecidomyiidae and Cynipidae, wherein the gall as a facility is better used for the nutrition and development of the immature stages of the inducing insect taxon. The gall-inducing insects are easy to monitor because of the distinct presence of galls, offering an advantage in extending in investigations about the eco-physiology of several other economically important, non-gall-inducing insects.The gall-inducing insects could be termed as ecosystem engineers in the sense that they manipulate plant architecture to create novel habitats. Their impacts on plants will continue to bear scrutiny, especially in regions where gall-inducing insects have been introduced and released from their natural enemies, thus potently threatening various other plants, including the economically relevant ones. © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved.

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DO - 10.1093/aesa/say034

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