Computational exploration of treadmilling and protrusion growth observed in fire ant rafts
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Evaluation Summary:
In this study, the authors present a numerical model of ant raft shape dynamics. It is an interesting topic, the experimental movies are exciting, and the idea that ant rafts make protrusions is new. The goal seems to be to explain how local interactions can lead to the perpetual protrusions of the raft. Since the biological significance of the results has not been clarified, the paper is likely to be primarily interesting to engineers and experts on robotics.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Collective living systems regularly achieve cooperative emergent functions that individual organisms could not accomplish alone. The rafts of fire ants (Solenopsis invicta) are often studied in this context for their ability to create aggregated structures comprised entirely of their own bodies, including tether-like protrusions that facilitate exploration of and escape from flooded environments. While similar protrusions are observed in cytoskeletons and cellular aggregates, they are generally dependent on morphogens or external gradients leaving the isolated role of local interactions poorly understood. Here we demonstrate through an ant-inspired, agent-based numerical model how protrusions in ant rafts may emerge spontaneously due to local interactions. The model is comprised of a condensed structural network of agents that represents the monolayer of interconnected worker ants, which floats on the water and gives ant rafts their form. Experimentally, this layer perpetually contracts, which we capture through the pairwise contraction of all neighboring structural agents at a strain rate of d ˙ . On top of the structural layer, we model a dispersed, on-lattice layer of motile agents that represents free ants, which walk on top of the floating network. Experimentally, these self-propelled free ants walk with some mean persistence length and speed that we capture through an ant-inspired phenomenological model. Local interactions occur between neighboring free ants within some radius of detection, R , and the persistence length of freely active agents is tuned through a noise parameter, η as introduced by the Vicsek model. Both R and η where fixed to match the experimental trajectories of free ants. Treadmilling of the raft occurs as agents transition between the structural and free layers in accordance with experimental observations. Ultimately, we demonstrate how phases of exploratory protrusion growth may be induced by increased ant activity as characterized by a dimensionless parameter, A . These results provide an example in which functional morphogenesis of a living system may emerge purely from local interactions at the constituent length scale, thereby providing a source of inspiration for the development of decentralized, autonomous active matter and swarm robotics.
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Evaluation Summary:
In this study, the authors present a numerical model of ant raft shape dynamics. It is an interesting topic, the experimental movies are exciting, and the idea that ant rafts make protrusions is new. The goal seems to be to explain how local interactions can lead to the perpetual protrusions of the raft. Since the biological significance of the results has not been clarified, the paper is likely to be primarily interesting to engineers and experts on robotics.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
This paper is well written, beautifully illustrated and appears to be a model of thoroughness. However, the paper does not convey an appropriate understanding of the biology of the behaviour described. Therefore, the paper is far more likely to be of interest to engineers and roboticists rather than biologists.
There is some conceptual overlap with previously published work:
Abstract:
Condensed active matter systems regularly achieve cooperative emergent functions that individual constituents could not accomplish alone." This general point was made in the Princeton monograph by Camazine et al. published in 2001, even though that book did not refer, of course to the new cliché of "condensed, active-matter systems". In general, it seems an oversight that Camazine et al. (2001) and associated work has not been …
Reviewer #1 (Public Review):
This paper is well written, beautifully illustrated and appears to be a model of thoroughness. However, the paper does not convey an appropriate understanding of the biology of the behaviour described. Therefore, the paper is far more likely to be of interest to engineers and roboticists rather than biologists.
There is some conceptual overlap with previously published work:
Abstract:
Condensed active matter systems regularly achieve cooperative emergent functions that individual constituents could not accomplish alone." This general point was made in the Princeton monograph by Camazine et al. published in 2001, even though that book did not refer, of course to the new cliché of "condensed, active-matter systems". In general, it seems an oversight that Camazine et al. (2001) and associated work has not been cited in this paper.
Discussion:
Our model indicates that fire ant rafts may exhibit spontaneous protrusion growth in the absence of external cues, long-range interactions, or centralized control and that the global response of these condensed active systems depends on the underlying behavior of individual constituents."
There is overlap with the work by Worley et al. (2019), who show in their paper on flocculation the adaptive value of a collective behaviour, which occurs in the absence of long-range interactions or centralised control, and that the global response depends on the underlying behaviour of the individual constituents (Worley A, Sendova-Franks AB, Franks NR. 2019 Social flocculation in plant-animal worms. R. Soc. open sci. 6: 181626. http://dx.doi.org/10.1098/rsos.181626).
In fairness, it could be that the originality of the current paper is that it shows collective phenomena in the absence of external cues. However, the paper states that worker activity level has a major influence over the formation of protrusions. Given that such worker activity is likely to be temperature dependent, then there is de facto an external cue, which would affect this claim to originality. Moreover, the growth of protrusions from a fire ant raft have not been shown to have any adaptive value at least in the current paper. So, the presence of absence of external cues does not appear necessarily to be of a great importance.
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Reviewer #2 (Public Review):
The authors present a numerical model of ant raft shape dynamics. It is an interesting topic, the experimental movies are exciting, and the idea that ant rafts make protrusions like this is new. The goal seems to be to explain how local interactions can lead to the perpetual protrusions of the raft. However, more efforts should be made to present probabillity distributions of the results rather than individual cases that happen to match the experiments.
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