Convergent evolution in silico reveals shape and dynamic principles of directed locomotion

Reviewer #1 (Public Review):

The manuscript presents a framework for studying biomechanical principles and their links to morphology and provides interesting insights into a particular question regarding terrestrial locomotion and speed. The goal of the paper is to derive general principles of directed terrestrial locomotion, speed, and symmetry.

Major strengths:
The manuscript is a unique and creative work that explores performance spaces of a complicated question through computational modeling. Overall, the paper is well written and well crafted and was a pleasure to read.

The methods presented here (variable agents used to represent ultra-simplified body configurations that are not inherently constrained) are interesting and there's significant potential in them for a properly constrained question. For the data that is present here their hypotheses (while they can be anticipated from first principles) are very well validated and serve as a robust validation of these expectations and can help.

Of particular interest was the discussion of the transferability of morphologies designed under one system and moving to another. From a deep-time perspective, of particular interest is the transition from subaqueous to terrestrial locomotion which we know was a major earth life transition. The results of this study show that the best-suited morphologies for subaqueous movement are ill-suited (from a locomotor speed standpoint at least) to fully terrestrial locomotion which begs the question of if there are a suite of forms that have balanced performance in both and how that would differ from aquatic morphologies.

Major weaknesses:
1. There is a major disagreement between the target and parameters.

From a biomechanics perspective the target of this study, Directed Locomotion, is a fairly broad behavioral mode. However, what the authors are ultimately evaluating their model organisms on is a single performance parameter (speed, or distance traveled after 30s). Statements such as "bilateral symmetry showed to be a law-like pattern in animal evolution for efficient directed locomotion purposes" (p 12 line 365-366) are problematic for this reason.

Attaining the highest possible speed is a relevant but limited subset of ways one might interpret performance for directed locomotion. Efficiency, power generation, and limb loading/strain are equally relevant components.

The focus on speed coupled with selection for only the highest performing morphologies, rather than setting a minimum performance threshold, fundamentally restricts the dynamics of the system in a way that is not representative of their specified target and pulls the simulations toward a specific, anticipatable, result.

Locomotor efficiency is alluded to later in the manuscript as one of the observed outcomes, but speed is not equivalent to locomotor efficiency (in much the same way that it is not the sole metric for describing performance with respect to directed locomotion). Energy/work/power have not been accounted for in the manuscript so this is not a parameter this study weighs in on.

The data and analyses the others present do show an interesting validation of these methods in assessing first-order questions relating the shape of a single performance surface to a theoretical morphology, which has significant potential value.

2. There is a significant population and/or sample size and biasing.

Thirty simulations of a population of 101 morphologies seems small for a study of this kind, particularly looking to investigate such a broad question at an abstract level. Particularly when the top 50% of morphologies are chosen to mutate. It would be very easy for artificial biases to rapidly propagate through this system depending on the parameters bounding the formation of the initial generation.

This strong selection choosing the best 50 morphologies and mutating them enforces an aggressive effect that simulates an even more potent phylogenetic inertia than one might anticipate for an actual evolutionary history (it's no surprise then that all of the simulations were able to successfully retrieve a suite of morphotypes that recovered the performance peak for this system within 1500 generations).

Similarly, why is it that a 4^3 voxel limit was chosen? One can imagine that an increase in this voxel limit would allow for the development of more extreme geometries, which might be successful. It is likely that there might be computational resource constraints involved in this, it would be useful for the authors to add additional context here.

Reviewer #2 (Public Review):

Acknowledging practical difficulties in teasing out the principles behind animal locomotion from the body's functions and survival needs, the authors embark on a computational experiment to replay the "tape of life." Specifically, the chief objective of the study was to explore the necessity of symmetry and modularity for better-directed locomotion on the ground.

Towards this important goal, the authors put forward a comprehensive computational study using physics-based simulations of 3D voxel-based robots. Such a simulation environment allows one to capture salient dynamics behind locomotion, including interactions with the environment. The authors undertake simulations for three different gravitational environments, water, Earth, and Mars. The work has several methodological strengths, with respect to the ingenuity of the approach and the elegance of the analysis; I was particularly intrigued by the use of graph theory in the context of modularity. Results point to a complex, rich role of modularity and symmetry in locomotion, modulated by the gravitational environment.

The association between "locomotion ability" and average speed is, in my view, tenuous, whereby locomotion is a complex phenomenon that should be assessed across a range of intertwined dynamic metrics that include, for example, stability with respect to external perturbations and energy efficiency. I also am not fully convinced of i) the adequacy of the spatial resolution, whereby I failed to see a compelling argument regarding the completeness of 64 voxels; ii) the realism of the oscillatory patterns, whereby all the voxels are set to oscillate at the same, constant, frequency of 2Hz; and iii) the accuracy of simulations in water where added mass effects seem to be neglected. Overall, dynamics and control aspects could be improved in both the methods and the interpretation of the results. Finally, I believe that a stronger connection between the hypotheses of the study and the literature (in animal or robot locomotion) would help frame the narrative better. I would be particularly curious to see some tie with human bipedal locomotion.

The work bears important implications in the study of locomotion, shedding light on the role of modularity and symmetry, beyond what one could gather from mere observations. Not only do I expect these new insights to stimulate further research in the area of locomotion, but also I envision other communities embracing a similar computational approach to address related questions in life sciences and robotics.