Cambrian origin of the arachnid brain.

Fossils from the lower Cambrian provide crucial insights into the diversification of arthropod lineages: Mandibulata, represented by centipedes, insects, and crustaceans; Chelicerata, represented by sea spiders, horseshoe crabs, and arachnids-the last including spiders, scorpions, and ticks. Two mid-Cambrian genera claimed as stem chelicerates are Mollisonia and Sanctacaris, defined by a carapaced prosoma equipped with clustered limbs, followed by a segmented trunk opisthosoma equipped with appendages for swimming and respiration. Until now, the phyletic status of Mollisoniidae and Sanctacarididae has been that of a basal chelicerate, stemward of Leanchoiliidae, whose neuromorphology resembles that of extant Merostomata (horseshoe crabs). Here, we identify preserved traces of neuronal tissues in Mollisonia symmetrica that crucially depart from a merostome organization. Instead, a radiating organization of metameric neuropils occupying most of its prosoma is situated behind a pair of oval unsegmented neuropils that are directly connected to paired chelicerae extending from the front of the prosoma. This connection identifies this neuropil pair as the deutocerebrum and signals a complete reversal of the order of the three genetically distinct domains that define euarthropod brains. In Mollisonia, the deutocerebrum is the most rostral cerebral domain. The proso- and protocerebral domains are folded backward such that tracts from the principal eyes extend caudally to reach their prosocerebral destination, itself having the unique disposition to interact directly with appendicular neuromeres. Phylogenetic analyses employing predominantly neural traits reveal Mollisonia symmetrica as an upper stem arachnid belonging to a lineage from which may have evolved the planet's most successful arthropodan predators.