Development of the Pre-gnathal Segments in the Milkweed Bug Oncopeltus fasciatus Suggests They Are Not Serial Homologs of Trunk Segments.

Oren Lev,Ariel D Chipman

doi:10.3389/fcell.2021.695135

Oren Lev, Ariel D Chipman

Open Access

https://doi.org/10.3389/fcell.2021.695135

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Abstract

The three anterior-most segments in arthropods contain the ganglia that make up the arthropod brain. These segments, the pre-gnathal segments (PGS), 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 conserved segment-polarity network, including genes from the Wnt and Hedgehog pathways, in the PGS, compared with the trunk segments, in the hemimetabolous insect Oncopeltus fasciatus. Gene function was tested by manipulating expression through RNA interference against components of the two pathways. We show that there are fundamental differences in the expression patterns of the segment polarity genes, in the timing of their expression and in the interactions among them in the process of pre-gnathal segment generation, relative to all other segments. We argue that given these differences, the PGS should not be considered serially homologous to trunk segments. This realization raises important questions about the differing evolutionary ancestry of different regions of the arthropod head.

Highlights

Arthropods are a hyper-diverse animal phylum characterized by both high species numbers and exceptional biomass
Comparing our findings to what is known from the literature, we argue that the pre-gnathal segments (PGS) in arthropods in general are patterned via a network that is different from that patterning the trunk segments
We started by looking at the expression of two of the segment polarity genes, hedgehog and wingless, from the earliest stages of formation of the PGS and up to the early segmented germband stage (Figure 1)

Summary

Introduction

Arthropods are a hyper-diverse animal phylum characterized by both high species numbers and exceptional biomass. The specifics of the segmentation process vary among species (Peel et al, 2005; Nagy and Williams, 2020) and can even vary within an individual embryo (Stahi and Chipman, 2016; Auman et al, 2017), core aspects of the process are highly conserved, and the segments are generally accepted to be homologous between all arthropods and serially homologous within an individual (Minelli and Fusco, 2013; Scholtz, 2020). This serial homology is usually taken to mean that they are patterned using a shared and conserved developmental process, namely, the aforementioned segmentation.

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