Tardigrades exhibit robust inter-limb coordination across walking speeds

Abstract

Tardigrades must negotiate heterogeneous, fluctuating environments, and accordingly utilize locomotive strategies capable of dealing with variable terrain. We analyze the kinematics and inter-leg coordination of freely walking tardigrades (species: Hypsibius dujardini). We find that tardigrade walking replicates several key features of walking in insects despite disparities in size, skeleton, and habitat. To test the effect of environmental changes on tardigrade locomotor control circuits, we measure kinematics and inter-leg coordination during walking on two substrates of different stiffnesses. We find that the phase offset between contralateral leg pairs is flexible, while ipsilateral coordination is preserved across environmental conditions. This mirrors similar results in insects and crustaceans. We propose that these functional similarities in walking coordination between tardigrades and arthropods is either due to a generalized locomotor control circuit common to panarthropods, or to independent convergence onto an optimal strategy for robust multi-legged control in small animals with simple circuitry. Our results highlight the value of tardigrades as a comparative system towards understanding the mechanisms -- neural and/or mechanical -- underlying coordination in panarthropod locomotion.

Universal Features in Panarthropod Inter-Limb Coordination during Forward Walking

“…All organisms surveyed display a smoothly decreasing duty factor with forward walking speed. Apart from the broadly observed negative correlation across species, the reported relationship between walking speed and duty factor varies in the literature (e.g., Wahl et al 2015 ; Weihmann et al 2017 ; Pfeffer et al 2019 ; Nirody et al 2021 ). In the absence of a generalizable underlying model (A constant swing duration and hyperbolic stance duration suggests a hyperbolic relationship between walking speed and duty factor.…”

“…Speed is largely modulated by changes in stance duration; in contrast, swing duration remains relatively constant over walking speeds, decreasing slowly with walking speed at low to medium speeds and leveling off at high speeds. Recent work has shown little correlation between swing duration and walking speed ( Wosnitza et al 2013 ; Nirody et al 2021 ) ( B ) The relative modulation of swing and stance duration within a stride is characterized by the duty factor, or proportion of a stride spent in stance. All organisms surveyed display a smoothly decreasing duty factor with forward walking speed.…”

“…All data shown for the tardigrade H. exemplaris were collected as reported in our previous work ( Nirody et al 2021 ). These data will be made available at http://www.github.com/jnirody/waterbears ; all other digitized data shown will be available at http://www.github.com/jnirody/invertICPs .…”

“…We attempt to include examples (and data) from a diversity of noninsect arthropods whenever possible. We present these alongside results from our investigations in the eutardigrade Hypsibius exemplaris ( Nirody et al 2021 ). We root our comparisons in a review of nervous system diversification across Panarthropoda ( Niven et al 2008 ; Carmen Ramona Smarandache-Wellmann 2016 ) noting, in particular, the similarities in VNC topology between tardigrades and arthopods ( Yang et al 2016 ).…”

The smooth transition from many-legged to bipedal locomotion - Gradual ground force reduction and its impact on total ground reaction forces, body dynamics and gait transitions

“…Evolution has brought forth similar rhythmic patterns of limb like appendages in a number of phylogenetically only loosely related groups, in which some have even evolved their legs independently of each other (e.g. (4,(11)(12)(13)(14)(15)). Manmade machines and models mostly adopt coordination patterns that closely mimic those found in animals.…”