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Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors.

ABSTRACT: The concerted evolution of morphological and behavioral specializations has compelling examples in ant castes. Unique to ants is a marked divergence between winged queens and wingless workers, but morphological specializations for behaviors on the ground have been overlooked. We analyzed thorax morphology of queens and workers in species from 21 of the 25 ant subfamilies. We uncovered unique skeletomuscular modifications in workers that presumably increase power and flexibility of head-thorax articulation, emphasizing that workers are not simply wingless versions of queens. We also identified two distinct types of queens and showed repeated evolutionary associations with strategies of colony foundation. Solitary founding queens that hunt have a more worker-like thorax. Our results reveal that ants invest in the relative size of thorax segments according to their tasks. Versatility of head movements allows for better manipulation of food and objects, which arguably contributed to the ants' ecological and evolutionary success. DOI: http://dx.doi.org/10.7554/eLife.01539.001.

SUBMITTER: Keller RA

PROVIDER: S-EPMC3881093 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors.

Keller Roberto A RA Peeters Christian C Beldade Patrícia P

eLife 20140107

The concerted evolution of morphological and behavioral specializations has compelling examples in ant castes. Unique to ants is a marked divergence between winged queens and wingless workers, but morphological specializations for behaviors on the ground have been overlooked. We analyzed thorax morphology of queens and workers in species from 21 of the 25 ant subfamilies. We uncovered unique skeletomuscular modifications in workers that presumably increase power and flexibility of head-thorax ar ...[more]

PMID: 24399458

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Project description:BackgroundExplanations 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.ResultsUsing 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.ConclusionsRather 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.

Project description:Insects breathe using a system of tracheal tubes that ramify throughout the body. Rhythmic tracheal compression (RTC), the periodic collapse and reinflation of parts of the system, has been identified in multiple taxa, but little is known about the precise dynamics of tube deformation cycles. It has been hypothesized that during RTC, compression occurs synchronously throughout the body, but specific kinematic patterns along the length of individual tracheae may vary. Tube collapse or reinflation that proceeds unidirectionally along the length of a tube may function as a pump to transport air, augmenting gas exchange. This study aims to characterize patterns of tracheal compression in one species of carabid beetle, Platynus decentis, to test the hypothesis of directional compression. The internal tracheae of living beetles were visualized using synchrotron x-ray phase contrast imaging at the Advanced Photon Source, Argonne National Laboratory. X-ray video results show that tracheal compression is characterized by the formation of discrete, buckled regions in the tube wall, giving the appearance of "dimpling." Dimple formation in the main dorsal tracheal trunks of the prothorax occurred as two semi-circular fronts that spread symmetrically or directionally along the longitudinal tube axis. In the transverse axis, the main ventral trunks collapsed in the lateral direction, whereas the dorsal trunks collapsed dorsoventrally. Along the length of the ventral thoracic tracheal trunks, collapse and reinflation occurred synchronously in the majority of cycles (75 percent), not sequentially. Synchronous longitudinal compression and consistent dimple formation kinematics within an animal suggest that Platynus decentis employs a stereotyped mechanism to produce cycles of tracheal collapse and reinflation, but such compression does not function as a unidirectional pump, at least along the length of the local trachea. Further data on spiracle opening and closing patterns and internal pressures within the tracheal system are required to determine actual airflow patterns within the body.

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Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors.

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Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors.

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