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The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour

dc.contributor.authorPeeters, Christian
dc.contributor.authorKeller, Roberto A.
dc.contributor.authorKhalife, Adam
dc.contributor.authorFischer, Georg
dc.contributor.authorKatzke, Julian
dc.contributor.authorBlanke, Alexander
dc.contributor.authorEconomo, Evan P.
dc.date.accessioned2024-02-08T15:34:48Z
dc.date.available2024-02-08T15:34:48Z
dc.date.issued2020
dc.description.abstractBackground Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. Results Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations resulting from the lack of wing muscles. Conclusions Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on morphological innovations of social insects to further our understanding of the evolution of social behaviours.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationPeeters, C., Keller, R. A., Khalife, A., Fischer, G., Katzke, J., Blanke, A., & Economo, E. P. (2020). The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour. Frontiers in Zoology, 17(1). https://doi.org/10.1186/s12983-020-00375-9pt_PT
dc.identifier.doi10.1186/s12983-020-00375-9pt_PT
dc.identifier.urihttp://hdl.handle.net/10451/62525
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherBMC Springer Naturept_PT
dc.relationEuropean Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No. 754290, “Mech-Evo-Insect”)pt_PT
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.titleThe loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labourpt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.citation.issue1pt_PT
oaire.citation.titleFrontiers in Zoologypt_PT
oaire.citation.volume17pt_PT
person.familyNameKeller Pérez
person.givenNameRoberto Andrés
person.identifier.ciencia-id6A11-8909-0DA6
person.identifier.orcid0000-0003-2751-9761
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
relation.isAuthorOfPublicatione9ed4df8-b7ec-4ba3-8138-7746975c0dcf
relation.isAuthorOfPublication.latestForDiscoverye9ed4df8-b7ec-4ba3-8138-7746975c0dcf

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