First 3-D reconstruction of copulation in Lepidoptera: interaction of genitalia in Tortrix viridana (Tortricidae).

CLSM Functional morphology Genitalia Green oak leafroller Micro-CT SEM

Journal

Frontiers in zoology
ISSN: 1742-9994
Titre abrégé: Front Zool
Pays: England
ID NLM: 101231669

Informations de publication

Date de publication:
11 Jul 2023
Historique:
received: 04 05 2023
accepted: 22 06 2023
medline: 12 7 2023
pubmed: 12 7 2023
entrez: 11 7 2023
Statut: epublish

Résumé

The process of copulation in Lepidoptera is understudied and poorly understood from a functional perspective. The purpose of the present paper is to study the interaction of the male and female genitalia of Tortrix viridana Linnaeus, 1758 via three-dimensional models of pairs fixed during copulation. Other techniques (confocal laser scanning microscopy, scanning electron microscopy and histology) were used to clarify the role of the organs involved in the process. Three-dimensional models based on micro-CT scanned copulating pairs were generated allowing visualisation of the position of the male and female counterparts, spatial changes during copulation, and the skeleto-muscular apparatus involved in the process. The male genitalia and their musculature are simplified in comparison with other lineages of the family, but the opposite is true for the female genitalia. The attachment of the couple is achieved only through flexion of the valvae, clasping the large and sclerotised sternite 7 of the female. The anal cone and socii of the male are in contact with certain parts of the anal papillae and the sterigma of the female. The long tubular vesica is inserted into the narrow posterior part of the ductus bursae. Its eversion is achieved by an increase in haemolymph pressure. A possible mechanism of stimulation of the female via pulsations of the diverticulum of the vesica was discovered. A compressed sclerotised area of the ductus bursae putatively serves as a valve controlling the transfer of ejaculated materials. Copulation progresses through two phases: in the first the vesica and its diverticulum are inflated by haemolymph, and in the second the diverticulum is not inflated, and the vesica is occupied by viscous ejaculated material. The formation of the multilayered spermatophore was observed, and we discovered that sperm is transferred very late in the copulation process. Copulation process in Lepidoptera is studied for the first time with three-dimensional reconstructions of couples of Tortrix viridana, used as a model species. The internal genitalia is the scenario of multiple interactions between male and female, but the external remain static. A possible mechanism of stimulation of the female internal copulation organs is proposed.

Sections du résumé

BACKGROUND BACKGROUND
The process of copulation in Lepidoptera is understudied and poorly understood from a functional perspective. The purpose of the present paper is to study the interaction of the male and female genitalia of Tortrix viridana Linnaeus, 1758 via three-dimensional models of pairs fixed during copulation. Other techniques (confocal laser scanning microscopy, scanning electron microscopy and histology) were used to clarify the role of the organs involved in the process.
RESULTS RESULTS
Three-dimensional models based on micro-CT scanned copulating pairs were generated allowing visualisation of the position of the male and female counterparts, spatial changes during copulation, and the skeleto-muscular apparatus involved in the process. The male genitalia and their musculature are simplified in comparison with other lineages of the family, but the opposite is true for the female genitalia. The attachment of the couple is achieved only through flexion of the valvae, clasping the large and sclerotised sternite 7 of the female. The anal cone and socii of the male are in contact with certain parts of the anal papillae and the sterigma of the female. The long tubular vesica is inserted into the narrow posterior part of the ductus bursae. Its eversion is achieved by an increase in haemolymph pressure. A possible mechanism of stimulation of the female via pulsations of the diverticulum of the vesica was discovered. A compressed sclerotised area of the ductus bursae putatively serves as a valve controlling the transfer of ejaculated materials. Copulation progresses through two phases: in the first the vesica and its diverticulum are inflated by haemolymph, and in the second the diverticulum is not inflated, and the vesica is occupied by viscous ejaculated material. The formation of the multilayered spermatophore was observed, and we discovered that sperm is transferred very late in the copulation process.
CONCLUSIONS CONCLUSIONS
Copulation process in Lepidoptera is studied for the first time with three-dimensional reconstructions of couples of Tortrix viridana, used as a model species. The internal genitalia is the scenario of multiple interactions between male and female, but the external remain static. A possible mechanism of stimulation of the female internal copulation organs is proposed.

Identifiants

pubmed: 37434159
doi: 10.1186/s12983-023-00500-4
pii: 10.1186/s12983-023-00500-4
pmc: PMC10334621
doi:

Types de publication

Journal Article

Langues

eng

Pagination

22

Subventions

Organisme : National Science Fund of Bulgaria
ID : КП-06-H31/4-10.12.2019

Informations de copyright

© 2023. The Author(s).

Références

Sci Rep. 2017 Feb 07;7:42345
pubmed: 28169372
Genetica. 2010 Jan;138(1):19-25
pubmed: 19089587
Stain Technol. 1955 Sep;30(5):209-12
pubmed: 13256167
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
J Morphol. 2002 Jun;252(3):298-314
pubmed: 11948677
Elife. 2017 Jun 21;6:
pubmed: 28636528
BMC Physiol. 2009 Jun 22;9:11
pubmed: 19545439
Insects. 2022 Aug 08;13(8):
pubmed: 36005339
J Morphol. 1988 Nov;198(2):231-241
pubmed: 29879791
Zootaxa. 2017 Jan 31;4227(1):zootaxa.4227.1.9
pubmed: 28187599
Zootaxa. 2016 Sep 15;4168(2):297-312
pubmed: 27701337

Auteurs

Boyan Zlatkov (B)

Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000, Sofia, Bulgaria. bzlatkov@gmail.com.

Vladislav Vergilov (V)

National Museum of Natural History, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000, Sofia, Bulgaria.

José Vicente Pérez Santa-Rita (JV)

Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Carrer Catedràtic José Beltran 2, 46980, Paterna, Spain.

Joaquín Baixeras (J)

Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Carrer Catedràtic José Beltran 2, 46980, Paterna, Spain.

Classifications MeSH