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Contribution to understanding the evolution of holometaboly: Transformation of internal head structures during the metamorphosis in the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)
Ding Yang
China Agricultural University
Corresponding Author
ORCiD: https://orcid.org/0000-0001-5963-4452
License:
This work is licensed under a CC BY 4.0 License. Read Full License
View the published version at BMC Ecology and Evolution.
Background：Metamorphosis remains one of the most complicated and poorly understood processes in insects. This is particularly so for the very dynamic transformations that take place within the pupal sheath of holometabolous insects. Only few studies address these transformations especially with regard to cranial structures of those holometabolous species where the larval and adult forms have a similar diet. It thus remains unclear to what extent the internal structures undergo histolysis and rebuilding. Here, the development of the brain and skeleto-muscular system of the head of Chrysopa pallens (Rambur, 1838) is studied. This species is a predator of aphids in the larval and adult stage.
Results：We used micro-computed-tomography (µ-CT) to study the transformations of the larval, prepupal and pupal head within the cocoon. We first assessed the morphological differences and similarities between the stages. We then determined the point in time when the compound eyes appear and describe the re-orientation of the head capsule which transforms the prognathous larva into a hypognathous adult. The internal head muscles are distinctly more slender in larvae than adults. In addition, the adults have a significantly larger brain which is likely needed for the processing of the signals obtained by the adults’ vastly expanded sensory organs that are presumably needed for dispersal and mating. Our study shows that the histolysis and modification of the inner muscles and skeletal elements take place within the prepupa. The central nervous system persists throughout metamorphosis but its morphology changes significantly.
Conclusion：Our study reveals that not only the inner structures, but also the outer morphology continues to change after the final larval moult. The adult cuticle and internal structures form gradually within the cocoon. The histolysis and rebuilding begins with the skeletal elements and is followed by changes in the central nervous system before it concludes with modifications of the musculature. This order of events is likely ancestral for Holometabola because it is also known from Hymenoptera, Diptera, Mecoptera, and Coleoptera.
Keywords
Chrysopidae, Neuroptera, 3D reconstruction, transformation
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CURRENT STATUS: Published
Version 2
Posted 11 May, 2020
Published
On 29 Jun, 2020
No community comments so far
Editorial decision: Accept
On 17 Jun, 2020
Review #1 received
Received 26 May, 2020
Review #2 received
Received 26 May, 2020
Reviewer #3 agreed
On 05 May, 2020
Reviewer #2 agreed
On 01 May, 2020
Editor assigned
On 30 Apr, 2020
Reviewers invited
Invitations sent on 30 Apr, 2020
Reviewer #1 agreed
On 30 Apr, 2020
Editor invited
On 29 Apr, 2020
Submission checks complete
On 26 Apr, 2020
No comments provided
Editorial decision: Major revision
On 27 Mar, 2020
Review #3 received
Received 26 Feb, 2020
Review #2 received
Received 18 Feb, 2020
Review #4 received
Received 18 Feb, 2020
Reviewer #4 agreed
On 07 Feb, 2020
Reviewer #3 agreed
On 05 Feb, 2020
Review #1 received
Received 13 Nov, 2019
Reviewers invited
Invitations sent on 11 Nov, 2019
Reviewer #1 agreed
On 11 Nov, 2019
Reviewer #2 agreed
On 11 Nov, 2019
Editor assigned
On 16 Oct, 2019
Submission checks complete
On 01 Oct, 2019
Editor invited
On 01 Oct, 2019
First submitted
On 23 Sep, 2019
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This preprint is under consideration at BMC Ecology and Evolution. A preprint is a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
Learn more about In Review
Research article
Contribution to understanding the evolution of holometaboly: Transformation of internal head structures during the metamorphosis in the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae)
Ding Yang
China Agricultural University
Corresponding Author
ORCiD: https://orcid.org/0000-0001-5963-4452
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
Prescreen
Peer Review Timeline
CURRENT STATUS: Published
Version 2
Posted 11 May, 2020
Published
On 29 Jun, 2020
No community comments so far
Editorial decision: Accept
On 17 Jun, 2020
Review #1 received
Received 26 May, 2020
Review #2 received
Received 26 May, 2020
Reviewer #3 agreed
On 05 May, 2020
Reviewer #2 agreed
On 01 May, 2020
Editor assigned
On 30 Apr, 2020
Reviewers invited
Invitations sent on 30 Apr, 2020
Reviewer #1 agreed
On 30 Apr, 2020
Editor invited
On 29 Apr, 2020
Submission checks complete
On 26 Apr, 2020
No comments provided
Editorial decision: Major revision
On 27 Mar, 2020
Review #3 received
Received 26 Feb, 2020
Review #2 received
Received 18 Feb, 2020
Review #4 received
Received 18 Feb, 2020
Reviewer #4 agreed
On 07 Feb, 2020
Reviewer #3 agreed
On 05 Feb, 2020
Review #1 received
Received 13 Nov, 2019
Reviewers invited
Invitations sent on 11 Nov, 2019
Reviewer #1 agreed
On 11 Nov, 2019
Reviewer #2 agreed
On 11 Nov, 2019
Editor assigned
On 16 Oct, 2019
Submission checks complete
On 01 Oct, 2019
Editor invited
On 01 Oct, 2019
First submitted
On 23 Sep, 2019
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
License:
This work is licensed under a CC BY 4.0 License. Read Full License
View the published version at BMC Ecology and Evolution.
Background：Metamorphosis remains one of the most complicated and poorly understood processes in insects. This is particularly so for the very dynamic transformations that take place within the pupal sheath of holometabolous insects. Only few studies address these transformations especially with regard to cranial structures of those holometabolous species where the larval and adult forms have a similar diet. It thus remains unclear to what extent the internal structures undergo histolysis and rebuilding. Here, the development of the brain and skeleto-muscular system of the head of Chrysopa pallens (Rambur, 1838) is studied. This species is a predator of aphids in the larval and adult stage.
Results：We used micro-computed-tomography (µ-CT) to study the transformations of the larval, prepupal and pupal head within the cocoon. We first assessed the morphological differences and similarities between the stages. We then determined the point in time when the compound eyes appear and describe the re-orientation of the head capsule which transforms the prognathous larva into a hypognathous adult. The internal head muscles are distinctly more slender in larvae than adults. In addition, the adults have a significantly larger brain which is likely needed for the processing of the signals obtained by the adults’ vastly expanded sensory organs that are presumably needed for dispersal and mating. Our study shows that the histolysis and modification of the inner muscles and skeletal elements take place within the prepupa. The central nervous system persists throughout metamorphosis but its morphology changes significantly.
Conclusion：Our study reveals that not only the inner structures, but also the outer morphology continues to change after the final larval moult. The adult cuticle and internal structures form gradually within the cocoon. The histolysis and rebuilding begins with the skeletal elements and is followed by changes in the central nervous system before it concludes with modifications of the musculature. This order of events is likely ancestral for Holometabola because it is also known from Hymenoptera, Diptera, Mecoptera, and Coleoptera.
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