ARTHROPOD EVOLUTION: PREDICTIONS FROM NEURAL CLADISTICS FIND SUPPORT IN BRAINS FROM THE CAMBRIAN

The nervous system provides one of the fundamental sources of data used for inferring the evolutionary relationships between major arthropod groups. Neural tissue is rarely preserved in fossil arthropods and thus stem- and early diverging crown-group taxa have hardly played a role in reconstructing the sequence of nervous system evolution in Arthropoda, or neural cladistics. Exceptional preservation of the brain and optic lobes of the 520 Ma stem-group arthropod Fuxianhuia protensa from the Chengjiang Lagerstätte reveals the most detailed neuroanatomy known from the Cambrian. The brain of Fuxianhuia has three neuromeres with connections to segmental structures: the protocerebrum is supplied by optic lobes retaining traces of nested neuropil areas that serve the eyes, the deutocerebum is defined by nerves from the antennae, and a contiguous tritocerebrum is indicated by a pair of more caudal nerves. A tripartite prestomodeal brain and three nested optic neuropils are shared with extant Malacostraca and Insecta but not Branchiopoda, which are inferred to have lost these and other brain centres such as olfactory lobes as secondary character reversals. Evidence from Fuxianhuia that stem arthropods possessed more elaborate brains than those of Branchiopoda is compounded by specimens of Waptia fieldensis from the Burgess Shale that demonstrate a single pair of antennae providing nerves to well-defined antennal lobes and compound eyes supplying optic stalk nerves that extend into a robust brain. Secondary simplification of the branchiopod brain reconciles neural cladistics with phylogenomic trees for Pancrustacea, which ally hexapods with remipedes. An early origin of sophisticated brains is coincident with versatile visual behaviours in Cambrian arthopods, as witnessed by the degree of rotational freedom in the stalked eyes of Fuxianhuia, as well by compound eyes of stem- and likely crown-group arthropods from the early Cambrian of Australia that were, in size and resolution, comparable to those of modern insects and malacostracans.