Collective behaviour in 480-million-year-old trilobite arthropods from Morocco

International audienceInteractions and coordination between conspecific individuals have produced a remarkable variety of collective behaviours. This cooperation occurs in vertebrate and invertebrate animals and is well expressed in the group flight of birds, fish shoals and highly organized activities of social insects. How individuals interact and why they cooperate to constitute group-level patterns has been extensively studied in extant animals through a variety mechanistic, functional and theoretical approaches. Although collective and social behaviour evolved through natural selection over millions of years, its origin and early history has remained largely unknown. In-situ monospecific linear clusters of trilobite arthropods from the lower Ordovician (ca 480 Ma) of Morocco are interpreted here as resulting either from a collective behaviour triggered by hydrodynamic cues in which mechanical stimulation detected by motion and touch sensors may have played a major role, or from a possible seasonal reproduction behaviour leading to the migration of sexually mature conspecifics to spawning grounds, possibly driven by chemical attraction (e.g. pheromones). This study confirms that collective behaviour has a very ancient origin and probably developed throughout the Cambrian-Ordovician interval, at the same time as the first animal radiation events. Modern arthropods provide numerous examples of collective behaviour 1 and group migrations. The pine proces-sionary caterpillars use pheromone trails and stimuli from abdominal setae to travel head to tail in large groups and over long distances in search of pupation sites (e.g. 2). Similarly, the non-flying juveniles of the desert locust 3-6 engage in gregarious behaviour to form huge mobile foraging groups in reaction to a set of mechanical, olfac-tory and visual stimuli associated with serotonin release 5. Collective behaviour also occurs in marine crustaceans such as spiny lobsters (Palinurus) which perform mass single-file migrations 7-11 across open substrates either in possible response to storm-induced environmental disturbances, or for reaching spawning grounds (Palinurus ornatus 12). Consistent directional positioning is maintained via tactile contact between followers and/ or possible chemical cues 13. Linear and unidirectional fossil clusters of conspecific trilobite arthropods occur in the Palaeozoic, which have been assumed to result from feeding, reproduction, moulting or sheltering behaviours 14-20. They have been also assumed to be a solution for reducing hydrodynamic drag effects within the moving groups 21. Much more enigmatic are the chain-like associations of bivalved euarthropods from the early Cambrian Chengjiang biota, which have been interpreted to have resulted from collective behaviour and tentatively compared with modern pelagic tunicate chains 22,23. Some non-linear trilobite clusters are seen as evidence for egg deposition in hatching sites 24 , others as resulting from hypothetical gatherings for protection or moulting 25. Most of these reported cases of linear or multidirectional clusters lack potentially important constraints on their interpretation such as the sedimentary environment where these animal groups lived and were buried. Here we describe and analyse quantitatively, numerous linear clusters of Ampyx priscus from the Lower Ordovician (upper Tremadocian-Floian, ca 480 Ma) Fezouata Shale of Morocco 26-29 , and show that these alignments of trilobites do not result from passive transportation and accumulation by currents but from a collectiv