Terebra steering in chalcidoid wasps

Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together wit...

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Published inFrontiers in zoology Vol. 20; no. 1; p. 26
Main Authors Eggs, Benjamin, Fischer, Stefan, Csader, Michael, Mikó, István, Rack, Alexander, Betz, Oliver
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 08.08.2023
BioMed Central
BMC
Subjects
Chalcidoidea
Diseases and pests
Drilling
Electronics industry
Employment
Females
Functional morphology
Host range
Host-parasite interactions
Hymenoptera
Investigations
Morphology
Muscles
Oviposition
Ovipositor
Parasitoid
Pteromalidae
Venom gland
Wasps
Japan
Germany
Ovipositor
Parasitoid
Pteromalidae
Hymenoptera
Functional morphology
Chalcidoidea
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Abstract Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together with videography, to analyse the musculoskeletal ovipositor system of the ectoparasitoid pteromalid wasp Lariophagus distinguendus (Förster, 1841) and the employment of its terebra during oviposition. The ovipositor consists of three pairs of valvulae, two pairs of valvifers and the female T9 (9th abdominal tergum). The paired 1st and the 2nd valvulae are interlocked via the olistheter system, which allows the three parts to slide longitudinally relative to each other, and form the terebra. The various ovipositor movements are actuated by a set of nine paired muscles, three of which (i.e. 1st valvifer-genital membrane muscle, ventral 2nd valvifer-venom gland reservoir muscle, T9-genital membrane muscle) are described here for the first time in chalcidoids. The anterior and posterior 2nd valvifer-2nd valvula muscles are adapted in function. (1) In the active probing position, they enable the wasps to pull the base of each of the longitudinally split and asymmetrically overlapping halves of the 2nd valvula that are fused at the apex dorsally, thus enabling lateral bending of the terebra. Concurrently, the 1st valvulae can be pro- and retracted regardless of this bending. (2) These muscles can also rotate the 2nd valvula and therefore the whole terebra at the basal articulation, allowing bending in various directions. The position of the terebra is anchored at the puncture site in hard substrates (in which drilling is extremely energy- and time-consuming). A freely steerable terebra increases the chance of contacting a potential host within a concealed cavity. The evolution of the ability actively to steer the terebra can be considered a key innovation that has putatively contributed to the acquisition of new hosts to a parasitoid's host range. Such shifts in host exploitation, each followed by rapid radiations, have probably aided the evolutionary success of Chalcidoidea (with more than 500,000 species estimated).
AbstractList Abstract Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together with videography, to analyse the musculoskeletal ovipositor system of the ectoparasitoid pteromalid wasp Lariophagus distinguendus (Förster, 1841) and the employment of its terebra during oviposition. The ovipositor consists of three pairs of valvulae, two pairs of valvifers and the female T9 (9th abdominal tergum). The paired 1st and the 2nd valvulae are interlocked via the olistheter system, which allows the three parts to slide longitudinally relative to each other, and form the terebra. The various ovipositor movements are actuated by a set of nine paired muscles, three of which (i.e. 1st valvifer-genital membrane muscle, ventral 2nd valvifer-venom gland reservoir muscle, T9-genital membrane muscle) are described here for the first time in chalcidoids. The anterior and posterior 2nd valvifer-2nd valvula muscles are adapted in function. (1) In the active probing position, they enable the wasps to pull the base of each of the longitudinally split and asymmetrically overlapping halves of the 2nd valvula that are fused at the apex dorsally, thus enabling lateral bending of the terebra. Concurrently, the 1st valvulae can be pro- and retracted regardless of this bending. (2) These muscles can also rotate the 2nd valvula and therefore the whole terebra at the basal articulation, allowing bending in various directions. The position of the terebra is anchored at the puncture site in hard substrates (in which drilling is extremely energy- and time-consuming). A freely steerable terebra increases the chance of contacting a potential host within a concealed cavity. The evolution of the ability actively to steer the terebra can be considered a key innovation that has putatively contributed to the acquisition of new hosts to a parasitoid’s host range. Such shifts in host exploitation, each followed by rapid radiations, have probably aided the evolutionary success of Chalcidoidea (with more than 500,000 species estimated).
Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together with videography, to analyse the musculoskeletal ovipositor system of the ectoparasitoid pteromalid wasp Lariophagus distinguendus (Förster, 1841) and the employment of its terebra during oviposition. The ovipositor consists of three pairs of valvulae, two pairs of valvifers and the female T9 (9th abdominal tergum). The paired 1st and the 2nd valvulae are interlocked via the olistheter system, which allows the three parts to slide longitudinally relative to each other, and form the terebra. The various ovipositor movements are actuated by a set of nine paired muscles, three of which (i.e. 1st valvifer-genital membrane muscle, ventral 2nd valvifer-venom gland reservoir muscle, T9-genital membrane muscle) are described here for the first time in chalcidoids. The anterior and posterior 2nd valvifer-2nd valvula muscles are adapted in function. (1) In the active probing position, they enable the wasps to pull the base of each of the longitudinally split and asymmetrically overlapping halves of the 2nd valvula that are fused at the apex dorsally, thus enabling lateral bending of the terebra. Concurrently, the 1st valvulae can be pro- and retracted regardless of this bending. (2) These muscles can also rotate the 2nd valvula and therefore the whole terebra at the basal articulation, allowing bending in various directions. The position of the terebra is anchored at the puncture site in hard substrates (in which drilling is extremely energy- and time-consuming). A freely steerable terebra increases the chance of contacting a potential host within a concealed cavity. The evolution of the ability actively to steer the terebra can be considered a key innovation that has putatively contributed to the acquisition of new hosts to a parasitoid's host range. Such shifts in host exploitation, each followed by rapid radiations, have probably aided the evolutionary success of Chalcidoidea (with more than 500,000 species estimated).
Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together with videography, to analyse the musculoskeletal ovipositor system of the ectoparasitoid pteromalid wasp Lariophagus distinguendus (Förster, 1841) and the employment of its terebra during oviposition. The ovipositor consists of three pairs of valvulae, two pairs of valvifers and the female T9 (9th abdominal tergum). The paired 1st and the 2nd valvulae are interlocked via the olistheter system, which allows the three parts to slide longitudinally relative to each other, and form the terebra. The various ovipositor movements are actuated by a set of nine paired muscles, three of which (i.e. 1st valvifer-genital membrane muscle, ventral 2nd valvifer-venom gland reservoir muscle, T9-genital membrane muscle) are described here for the first time in chalcidoids. The anterior and posterior 2nd valvifer-2nd valvula muscles are adapted in function. (1) In the active probing position, they enable the wasps to pull the base of each of the longitudinally split and asymmetrically overlapping halves of the 2nd valvula that are fused at the apex dorsally, thus enabling lateral bending of the terebra. Concurrently, the 1st valvulae can be pro- and retracted regardless of this bending. (2) These muscles can also rotate the 2nd valvula and therefore the whole terebra at the basal articulation, allowing bending in various directions. The position of the terebra is anchored at the puncture site in hard substrates (in which drilling is extremely energy- and time-consuming). A freely steerable terebra increases the chance of contacting a potential host within a concealed cavity. The evolution of the ability actively to steer the terebra can be considered a key innovation that has putatively contributed to the acquisition of new hosts to a parasitoid's host range. Such shifts in host exploitation, each followed by rapid radiations, have probably aided the evolutionary success of Chalcidoidea (with more than 500,000 species estimated). Keywords: Chalcidoidea, Functional morphology, Hymenoptera, Ovipositor, Parasitoid, Pteromalidae
Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together with videography, to analyse the musculoskeletal ovipositor system of the ectoparasitoid pteromalid wasp Lariophagus distinguendus (Förster, 1841) and the employment of its terebra during oviposition. The ovipositor consists of three pairs of valvulae, two pairs of valvifers and the female T9 (9th abdominal tergum). The paired 1st and the 2nd valvulae are interlocked via the olistheter system, which allows the three parts to slide longitudinally relative to each other, and form the terebra. The various ovipositor movements are actuated by a set of nine paired muscles, three of which (i.e. 1st valvifer-genital membrane muscle, ventral 2nd valvifer-venom gland reservoir muscle, T9-genital membrane muscle) are described here for the first time in chalcidoids. The anterior and posterior 2nd valvifer-2nd valvula muscles are adapted in function. (1) In the active probing position, they enable the wasps to pull the base of each of the longitudinally split and asymmetrically overlapping halves of the 2nd valvula that are fused at the apex dorsally, thus enabling lateral bending of the terebra. Concurrently, the 1st valvulae can be pro- and retracted regardless of this bending. (2) These muscles can also rotate the 2nd valvula and therefore the whole terebra at the basal articulation, allowing bending in various directions. The position of the terebra is anchored at the puncture site in hard substrates (in which drilling is extremely energy- and time-consuming). A freely steerable terebra increases the chance of contacting a potential host within a concealed cavity. The evolution of the ability actively to steer the terebra can be considered a key innovation that has putatively contributed to the acquisition of new hosts to a parasitoid’s host range. Such shifts in host exploitation, each followed by rapid radiations, have probably aided the evolutionary success of Chalcidoidea (with more than 500,000 species estimated).
Abstract Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To investigate the mechanisms of these bending and rotational movements, we combined microscopical and microtomographical techniques, together with videography, to analyse the musculoskeletal ovipositor system of the ectoparasitoid pteromalid wasp Lariophagus distinguendus (Förster, 1841) and the employment of its terebra during oviposition. The ovipositor consists of three pairs of valvulae, two pairs of valvifers and the female T9 (9th abdominal tergum). The paired 1st and the 2nd valvulae are interlocked via the olistheter system, which allows the three parts to slide longitudinally relative to each other, and form the terebra. The various ovipositor movements are actuated by a set of nine paired muscles, three of which (i.e. 1st valvifer-genital membrane muscle, ventral 2nd valvifer-venom gland reservoir muscle, T9-genital membrane muscle) are described here for the first time in chalcidoids. The anterior and posterior 2nd valvifer-2nd valvula muscles are adapted in function. (1) In the active probing position, they enable the wasps to pull the base of each of the longitudinally split and asymmetrically overlapping halves of the 2nd valvula that are fused at the apex dorsally, thus enabling lateral bending of the terebra. Concurrently, the 1st valvulae can be pro- and retracted regardless of this bending. (2) These muscles can also rotate the 2nd valvula and therefore the whole terebra at the basal articulation, allowing bending in various directions. The position of the terebra is anchored at the puncture site in hard substrates (in which drilling is extremely energy- and time-consuming). A freely steerable terebra increases the chance of contacting a potential host within a concealed cavity. The evolution of the ability actively to steer the terebra can be considered a key innovation that has putatively contributed to the acquisition of new hosts to a parasitoid’s host range. Such shifts in host exploitation, each followed by rapid radiations, have probably aided the evolutionary success of Chalcidoidea (with more than 500,000 species estimated).
ArticleNumber 26
Audience Academic
Author Mikó, István
Csader, Michael
Betz, Oliver
Fischer, Stefan
Rack, Alexander
Eggs, Benjamin
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  organization: Evolutionary Biology of Invertebrates, Institute of Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 28, 72076, Tübingen, Germany. benjamin.eggs@uni-tuebingen.de
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  surname: Fischer
  fullname: Fischer, Stefan
  organization: Tübingen Structural Microscopy Core Facility (TSM), University of Tübingen, Schnarrenbergstraße 94-96, 72076, Tübingen, Germany
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  givenname: Michael
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  surname: Csader
  fullname: Csader, Michael
  organization: State Museum of Natural History Karlsruhe, Erbprinzenstraße 13, 76133, Karlsruhe, Germany
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  surname: Mikó
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  organization: Department of Biological Sciences, University of New Hampshire Collection of Insects and Other Arthropods, University of New Hampshire, Spaulding Hall, Durham, NH, 03824, USA
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  givenname: Alexander
  orcidid: 0000-0001-9486-3621
  surname: Rack
  fullname: Rack, Alexander
  organization: ESRF - The European Synchrotron, Structure of Materials Group - ID19, CS 40220, 38043, Grenoble Cedex 9, France
– sequence: 6
  givenname: Oliver
  orcidid: 0000-0002-5012-4808
  surname: Betz
  fullname: Betz, Oliver
  organization: Evolutionary Biology of Invertebrates, Institute of Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 28, 72076, Tübingen, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37553687$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Ovipositor
Parasitoid
Pteromalidae
Hymenoptera
Functional morphology
Chalcidoidea
Language English
License 2023. BioMed Central Ltd., part of Springer Nature.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
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Snippet Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To...
Abstract Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic...
Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic musculature. To...
Abstract Various chalcidoid wasps can actively steer their terebra (= ovipositor shaft) in diverse directions, despite the lack of terebral intrinsic...
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StartPage 26
SubjectTerms Chalcidoidea
Diseases and pests
Drilling
Electronics industry
Employment
Females
Functional morphology
Host range
Host-parasite interactions
Hymenoptera
Investigations
Morphology
Muscles
Oviposition
Ovipositor
Parasitoid
Pteromalidae
Venom gland
Wasps
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Title Terebra steering in chalcidoid wasps
URI https://www.ncbi.nlm.nih.gov/pubmed/37553687
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https://doaj.org/article/e05cc3c14c964f1eaa8db27d9ccb27e4
Volume 20
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