Cargando…

Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants

Jumping is a rapid locomotory mode widespread in terrestrial organisms. However, it is a rare specialization in ants. Forward jumping has been reported within four distantly related ant genera: Gigantiops, Harpegnathos, Myrmecia, and Odontomachus. The temporal engagement of legs/body parts during ju...

Descripción completa

Detalles Bibliográficos
Autores principales: Aibekova, L, Keller, R A, Katzke, J, Allman, D M, Hita-Garcia, F, Labonte, D, Narendra, A, Economo, E P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10401624/
https://www.ncbi.nlm.nih.gov/pubmed/37545740
http://dx.doi.org/10.1093/iob/obad026
_version_ 1785084706627256320
author Aibekova, L
Keller, R A
Katzke, J
Allman, D M
Hita-Garcia, F
Labonte, D
Narendra, A
Economo, E P
author_facet Aibekova, L
Keller, R A
Katzke, J
Allman, D M
Hita-Garcia, F
Labonte, D
Narendra, A
Economo, E P
author_sort Aibekova, L
collection PubMed
description Jumping is a rapid locomotory mode widespread in terrestrial organisms. However, it is a rare specialization in ants. Forward jumping has been reported within four distantly related ant genera: Gigantiops, Harpegnathos, Myrmecia, and Odontomachus. The temporal engagement of legs/body parts during jump, however, varies across these genera. It is unknown what morphological adaptations underlie such behaviors and whether jumping in ants is solely driven directly by muscle contraction or additionally relies on elastic recoil mechanism. We investigated the morphological adaptations for jumping behavior by comparing differences in the locomotory musculature between jumping and non-jumping relatives using X-ray micro-CT and 3D morphometrics. We found that the size-specific volumes of the trochanter depressor muscle (scm6) of the middle and hind legs are 3–5 times larger in jumping ants, and that one coxal remotor muscle (scm2) is reduced in volume in the middle and/or hind legs. Notably, the enlargement in the volume of other muscle groups is directly linked to the legs or body parts engaged during the jump. Furthermore, a direct comparison of the muscle architecture revealed two significant differences between jumping vs. non-jumping ants: First, the relative Physiological Cross-Sectional Area (PCSA) of the trochanter depressor muscles of all three legs were larger in jumping ants, except in the front legs of Odontomachus rixosus and Myrmecia nigrocincta; second, the relative muscle fiber length was shorter in jumping ants compared to non-jumping counterparts, except in the front legs of O. rixosus and M. nigrocincta. These results suggest that the difference in relative muscle volume in jumping ants is largely invested in the area (PCSA), and not in fiber length. There was no clear difference in the pennation angle between jumping and non-jumping ants. Additionally, we report that the hind leg length relative to body length was longer in jumping ants. Based on direct comparison of the observed vs. possible work and power output during jumps, we surmise that direct muscle contractions suffice to explain jumping performance in three species, except for O. rixosus, where the lack of data on jumping performance prevents us from drawing definitive conclusions for this particular species. We suggest that increased investment in jumping-relevant musculature is a primary morphological adaptation that separates jumping from non-jumping ants. These results elucidate the common and idiosyncratic morphological changes underlying this rare adaptation in ants. まとぅみ (Okinawan language—Uchinaaguchi) [Image: see text] 要旨 (Japanese) [Image: see text] РЕЗЮМЕ (Kazakh) [Image: see text] ZUSAMMENFASSUNG (German) [Image: see text]
format Online
Article
Text
id pubmed-10401624
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-104016242023-08-05 Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants Aibekova, L Keller, R A Katzke, J Allman, D M Hita-Garcia, F Labonte, D Narendra, A Economo, E P Integr Org Biol Article Jumping is a rapid locomotory mode widespread in terrestrial organisms. However, it is a rare specialization in ants. Forward jumping has been reported within four distantly related ant genera: Gigantiops, Harpegnathos, Myrmecia, and Odontomachus. The temporal engagement of legs/body parts during jump, however, varies across these genera. It is unknown what morphological adaptations underlie such behaviors and whether jumping in ants is solely driven directly by muscle contraction or additionally relies on elastic recoil mechanism. We investigated the morphological adaptations for jumping behavior by comparing differences in the locomotory musculature between jumping and non-jumping relatives using X-ray micro-CT and 3D morphometrics. We found that the size-specific volumes of the trochanter depressor muscle (scm6) of the middle and hind legs are 3–5 times larger in jumping ants, and that one coxal remotor muscle (scm2) is reduced in volume in the middle and/or hind legs. Notably, the enlargement in the volume of other muscle groups is directly linked to the legs or body parts engaged during the jump. Furthermore, a direct comparison of the muscle architecture revealed two significant differences between jumping vs. non-jumping ants: First, the relative Physiological Cross-Sectional Area (PCSA) of the trochanter depressor muscles of all three legs were larger in jumping ants, except in the front legs of Odontomachus rixosus and Myrmecia nigrocincta; second, the relative muscle fiber length was shorter in jumping ants compared to non-jumping counterparts, except in the front legs of O. rixosus and M. nigrocincta. These results suggest that the difference in relative muscle volume in jumping ants is largely invested in the area (PCSA), and not in fiber length. There was no clear difference in the pennation angle between jumping and non-jumping ants. Additionally, we report that the hind leg length relative to body length was longer in jumping ants. Based on direct comparison of the observed vs. possible work and power output during jumps, we surmise that direct muscle contractions suffice to explain jumping performance in three species, except for O. rixosus, where the lack of data on jumping performance prevents us from drawing definitive conclusions for this particular species. We suggest that increased investment in jumping-relevant musculature is a primary morphological adaptation that separates jumping from non-jumping ants. These results elucidate the common and idiosyncratic morphological changes underlying this rare adaptation in ants. まとぅみ (Okinawan language—Uchinaaguchi) [Image: see text] 要旨 (Japanese) [Image: see text] РЕЗЮМЕ (Kazakh) [Image: see text] ZUSAMMENFASSUNG (German) [Image: see text] Oxford University Press 2023-07-25 /pmc/articles/PMC10401624/ /pubmed/37545740 http://dx.doi.org/10.1093/iob/obad026 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Article
Aibekova, L
Keller, R A
Katzke, J
Allman, D M
Hita-Garcia, F
Labonte, D
Narendra, A
Economo, E P
Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants
title Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants
title_full Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants
title_fullStr Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants
title_full_unstemmed Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants
title_short Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants
title_sort parallel and divergent morphological adaptations underlying the evolution of jumping ability in ants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10401624/
https://www.ncbi.nlm.nih.gov/pubmed/37545740
http://dx.doi.org/10.1093/iob/obad026
work_keys_str_mv AT aibekoval parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT kellerra parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT katzkej parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT allmandm parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT hitagarciaf parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT labonted parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT narendraa parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants
AT economoep parallelanddivergentmorphologicaladaptationsunderlyingtheevolutionofjumpingabilityinants