Marine Origin of the Arachnid Brain Reveals Early Divergence of Chelicerata

Abstract

Fossils from the lower Cambrian provide crucial insights into the diversification of arthropod lineages: Mandibulata, exemplified by centipedes, insects, and crustaceans; and Chelicerata, represented by sea spiders, horseshoe crabs, and arachnids, the last including spiders, scorpions, and ticks1. 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 respiration2-4. Up to the present, the phyletic status of Mollisoniidae and Sanctacariidae has been that of a basal chelicerate2, stemward of Leanchoiliidae, whose neuromorphology resembles that of extant Merostomata (horseshoe crabs)5. 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 directly connected to paired chelicerae extending from the front of the prosoma. The disposition and connections of these neuropils is the neuroanatomical signature that denotes a complete reversal of the three genetically distinct domains defining arthropod brains6. Thus, in Mollisonia the deutocerebrum is the most rostral domain with the proso-and protocerebral domains folded backwards such that tracts from the principal eyes extend caudally to reach their prosocerebral destination. These defining neuromorphological features illuminate a marine origin of Arachnida from which evolved the planets most successful arthropodan predators.