Social behaviour and collective motion in plant-animal worms

Abstract

Social behaviour may enable organisms to occupy ecological niches that would otherwise be unavailable to them. Here, we test this major evolutionary principle by demonstrating self-organizing social behaviour in the plant-animal, Symsagittifera roscoffensis. These marine aceol flat worms rely for all of their nutrition on the algae within their bodies: hence their common name. We show that individual worms interact with one another to coordinate their movements so that even at low densities they begin to swim in small polarized groups and at increasing densities such flotillas turn into circular mills. We use computer simulations to: (i) determine if real worms interact socially by comparing them with virtual worms that do not interact and (ii) show that the social phase transitions of the real worms can occur based only on local interactions between and among them. We hypothesize that such social behaviour helps the worms to form the dense biofilms or mats observed on certain sunexposed sandy beaches in the upper intertidal of the East Atlantic and to become in effect a super-organismic seaweed in a habitat where macro-algal seaweeds cannot anchor themselves. Symsagittifera roscoffensis, a model organism in many other areas in biology (including stem cell regeneration), also seems to be an ideal model for understanding how individual behaviours can lead, through collective movement, to social assemblages.

Xenacoelomorpha's significance for understanding bilaterian evolution

“…In some lineages anterior condensations have been internalized to form a brain, and bundles of longitudinal nerves have been multiplied and internalized to form nerve cords [13,39 ]. These modifications correlate with an elaboration of the behavioral complexity in the Acoela, such as swimming in threedimensional interstitial environment, circadian rhythms, active predation, and swarm behavior [42,43].…”

An Emerging System to Study Photosymbiosis, Brain Regeneration, Chronobiology, and Behavior: The Marine Acoel Symsagittifera roscoffensis

“…The availability of large numbers of animals that can easily be collected in nature, transported, and maintained for weeks to months, make S. roscoffensis amenable for behavioral studies. They exhibit a behavioral repertoire that includes phototaxis, geotaxis, rheotaxis, thermotaxis, responses to mechanical stimulation and vibration, and even social responses influenced by the presence of conspecifics . The majority of experimental evidence was obtained over a century ago, and there is therefore considerable scope for further exploration with modern technologies and novel hypotheses.…”

“…In terms of responses to mechanical stimulation and vibration, it is robustly and stereotypically displayed in adults by a body contraction behavior, which remains unchanged even in the absence of the brain (i.e., after decapitation) . Symsagittifera roscoffensis has also been posited as an ideal system to study how individual behaviors can lead, through collective movement, to social assemblages . When placed on a horizontal surface, adults actively interact with their neighbors, leading to a clock‐wise circular milling aggregation behavior that might be related to photoprotection by shading each other .…”

“…They exhibit a behavioral repertoire that includes phototaxis, [21,40,59] geotaxis, [3,57] rheotaxis, [59] thermotaxis, [59] responses to mechanical stimulation and vibration, [40] and even social responses influenced by the presence of conspecifics. [60] The majority of experimental evidence was obtained over a century ago, and there is therefore considerable scope for further exploration with modern technologies and novel hypotheses.…”

Understanding how animal groups achieve coordinated movement

“…Collective motion also emerges through antagonistic contacts between individuals, such as when Mormon crickets ( Anabrus simplex ) or juvenile desert locusts ( Schistocerca gregaria ) chase and avoid conspecifics in cannibalistic interactions (Simpson et al, 2006; Bazazi et al, 2008; Hansen et al, 2011). The reasons that other animals move in groups remain unresolved; for example, at high densities, plant–animal worms ( Symsagittifera roscoffensis ) form rotating mills, the function of which remains unclear (Franks et al, 2016). In other systems, collective motion may emerge through repeated interactions between individuals in confined environments (Mann et al, 2013).…”