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Developmental biomechanics and age polyethism in leaf-cutter ants

Frederik Püffel Orcid Logo, Lara Meyer, Natalie Imirzian, Flavio Roces, Richard Johnston Orcid Logo, David Labonte Orcid Logo

Proceedings of the Royal Society B: Biological Sciences, Volume: 290, Issue: 2000

Swansea University Author: Richard Johnston Orcid Logo

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DOI (Published version): 10.1098/rspb.2023.0355

Abstract

Many social insects display age polyethism: young workers stay inside the nest, and only older workers forage. This behavioural transition is accompanied by genetic and physiological changes, but the mechanistic origin of it remains unclear. To investigate if the mechanical demands on the musculoske...

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Published in: Proceedings of the Royal Society B: Biological Sciences
ISSN: 0962-8452 1471-2954
Published: The Royal Society 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa63729
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spelling v2 63729 2023-06-28 Developmental biomechanics and age polyethism in leaf-cutter ants 23282e7acce87dd926b8a62ae410a393 0000-0003-1977-6418 Richard Johnston Richard Johnston true false 2023-06-28 MTLS Many social insects display age polyethism: young workers stay inside the nest, and only older workers forage. This behavioural transition is accompanied by genetic and physiological changes, but the mechanistic origin of it remains unclear. To investigate if the mechanical demands on the musculoskeletal system effectively prevent young workers from foraging, we studied the biomechanical development of the bite apparatus in Atta vollenweideri leaf-cutter ants. Fully matured foragers generated peak in vivo bite forces of around 100 mN, more than one order of magnitude in excess of those measured for freshly eclosed callows of the same size. This change in bite force was accompanied by a sixfold increase in the volume of the mandible closer muscle, and by a substantial increase of the flexural rigidity of the head capsule, driven by a significant increase in both average thickness and indentation modulus of the head capsule cuticle. Consequently, callows lack the muscle force capacity required for leaf-cutting, and their head capsule is so compliant that large muscle forces would be likely to cause damaging deformations. On the basis of these results, we speculate that continued biomechanical development post eclosion may be a key factor underlying age Journal Article Proceedings of the Royal Society B: Biological Sciences 290 2000 The Royal Society 0962-8452 1471-2954 division of labour, behavioural development, social insects, bite forces 14 6 2023 2023-06-14 10.1098/rspb.2023.0355 http://dx.doi.org/10.1098/rspb.2023.0355 COLLEGE NANME Materials Science and Engineering COLLEGE CODE MTLS Swansea University Another institution paid the OA fee This study is part of a project that has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 851705) awarded to D.L. 2023-11-15T12:28:00.5488024 2023-06-28T10:13:52.9201308 Faculty of Science and Engineering School of Engineering and Applied Sciences - Materials Science and Engineering Frederik Püffel 0000-0002-3917-0942 1 Lara Meyer 2 Natalie Imirzian 3 Flavio Roces 4 Richard Johnston 0000-0003-1977-6418 5 David Labonte 0000-0002-1952-8732 6 63729__27995__4ebdbc8f26d046daaa16dec65cec7634.pdf 63729.pdf 2023-06-28T10:18:28.3538728 Output 851372 application/pdf Version of Record true Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. true eng http://creativecommons.org/licenses/by/4.0/
title Developmental biomechanics and age polyethism in leaf-cutter ants
spellingShingle Developmental biomechanics and age polyethism in leaf-cutter ants
Richard Johnston
title_short Developmental biomechanics and age polyethism in leaf-cutter ants
title_full Developmental biomechanics and age polyethism in leaf-cutter ants
title_fullStr Developmental biomechanics and age polyethism in leaf-cutter ants
title_full_unstemmed Developmental biomechanics and age polyethism in leaf-cutter ants
title_sort Developmental biomechanics and age polyethism in leaf-cutter ants
author_id_str_mv 23282e7acce87dd926b8a62ae410a393
author_id_fullname_str_mv 23282e7acce87dd926b8a62ae410a393_***_Richard Johnston
author Richard Johnston
author2 Frederik Püffel
Lara Meyer
Natalie Imirzian
Flavio Roces
Richard Johnston
David Labonte
format Journal article
container_title Proceedings of the Royal Society B: Biological Sciences
container_volume 290
container_issue 2000
publishDate 2023
institution Swansea University
issn 0962-8452
1471-2954
doi_str_mv 10.1098/rspb.2023.0355
publisher The Royal Society
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Engineering and Applied Sciences - Materials Science and Engineering{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Engineering and Applied Sciences - Materials Science and Engineering
url http://dx.doi.org/10.1098/rspb.2023.0355
document_store_str 1
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description Many social insects display age polyethism: young workers stay inside the nest, and only older workers forage. This behavioural transition is accompanied by genetic and physiological changes, but the mechanistic origin of it remains unclear. To investigate if the mechanical demands on the musculoskeletal system effectively prevent young workers from foraging, we studied the biomechanical development of the bite apparatus in Atta vollenweideri leaf-cutter ants. Fully matured foragers generated peak in vivo bite forces of around 100 mN, more than one order of magnitude in excess of those measured for freshly eclosed callows of the same size. This change in bite force was accompanied by a sixfold increase in the volume of the mandible closer muscle, and by a substantial increase of the flexural rigidity of the head capsule, driven by a significant increase in both average thickness and indentation modulus of the head capsule cuticle. Consequently, callows lack the muscle force capacity required for leaf-cutting, and their head capsule is so compliant that large muscle forces would be likely to cause damaging deformations. On the basis of these results, we speculate that continued biomechanical development post eclosion may be a key factor underlying age
published_date 2023-06-14T12:28:03Z
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