Development of the Pre-Gnathal Segments of the Insect Head Indicates They Are Not Serial Homologues of Trunk Segments

Abstract

The three anterior-most segments in arthropods contain the ganglia that make up the arthropod brain. These segments, the pre-gnathal segments, are known to exhibit many developmental differences to other segments, believed to reflect their divergent morphology. We have analyzed the expression and function of the genes involved in the segment-polarity network in the pre-gnathal segments compared with the trunk segments in the hemimetabolous insect Oncopeltus fasciatus. We show that there are fundamental differences in the way the pre-gnathal segments are generated and patterned, relative to all other segments, and that these differences are general to all arthropods. We argue that given these differences, the pre-gnathal segments should not be considered serially homologous to trunk segments. This realization has important implications for our understanding of the evolution of the arthropod head. We suggest a novel scenario for arthropod head evolution that posits duplication of an ancestral single-segmented head into three descendent segments. This scenario is consistent with what we know of head evolution from the fossil record, and helps reconcile some of the debates about early arthropod evolution.

The origin and early evolution of arthropods

“…Perhaps the zealousness in homologizing the tripartite brain (protocerebrum, deutocerebrum, tritocerebrum) in fossil taxa (Ortega-Hernández et al 2017) could also be mitigated by the consideration that the morpho-anatomy of the brain itself has evolved, and therefore that brain subdivisions in fossils (in the form of fused and emerging ganglia) could mislead topological alignments based on extant taxa. A current investigation may provide developmental evidence to support this view (Lev and Chipman 2020). Some authors have also generally rejected the palaeoneurological evidence based on the frailty of such internal tissues as ganglions and nerves and their high susceptibility to decay (Liu et al 2018).…”