Nasoniasegmentation is regulated by an ancestral insect segmentation regulatory network also present in flies

Abstract

Insect segmentation is a well-studied and tractable system with which to investigate the genetic regulation of development. Though insects segment their germband using a variety of methods, modelling work implies that a single gene regulatory network can underpin the two main types of insect segmentation. This means limited genetic changes are required to explain significant differences in segmentation mode between different insects. Evidence for this idea is limited to Drosophila melanogaster, Tribolium castaneum, and the spider Parasteatoda tepidariorum, and the nature of the gene regulatory network (GRN) underlying this model has not been tested. Some insects, for example Nasonia vitripennis and Apis mellifera segment progressively, a pattern not examined in studies of this segmentation model, producing stripes at different times throughout the embryo, but not from a segment addition zone. Here we aim to understand the GRNs patterning Nasonia using a simulation-based approach. We found that an existing model of Drosophila segmentation (Clark 2017) can be used to recapitulate Nasonia's progressive segmentation, if provided with altered inputs in the form of expression of the timer genes Nv-caudal and Nv-odd paired. We also predict limited topological changes to the pair rule network. Together this implies that very limited changes to the Drosophila network are required to simulate Nasonia segmentation, despite the differences in segmentation modes, implying that Nasonia use a very similar version of an ancestral GRN also used by Drosophila.

Anterior‐posterior patterning of segments in Anopheles stephensi offers insights into the transition from sequential to simultaneous segmentation in holometabolous insects

“…This wavelike pattern of opa can explain the gradual transition from pair-rule to segment polarity type patterns. A similarly shifting opa expression pattern has recently been described in Nasonia, which undergoes progressive segmentation in the anterior portion of its trunk (Taylor & Dearden, 2021). This is suggestive of a common timing mechanism used in long-germ insects to achieve progressive segmentation which was modified in the lineage leading to Drosophila to promote simultaneous segmentation.…”

“…Even though the term “progressive segmentation” is newly adopted, an analysis of older studies indicates that it likely applies to many of the holometabolous long‐germ insects (Figure 6b). Anterior‐posterior addition of pair‐rule stripes has been observed in the Lepidopteran Bombyx mori (Nakao, 2010, 2015; Xu et al, 1997), the Hymenoptera Apis mellifera (Binner & Sander, 1997; Wilson & Dearden, 2012), and N. vitripennis (Taylor & Dearden, 2021), the Coleopteran Callosobruchus maculatus (Patel et al, 1994), and Nematocera (Diptera) Clogmia albipunctata and Coboldia fuscipes (Bullock et al, 2004; Rohr et al, 1999) (Figure 6b). In many of these species, the eve pair‐rule pattern is not complete before gastrulation.…”

“…Another distinction between these modes is that segment patterning is complete before gastrulation for simultaneous segmentation but is ongoing throughout germband elongation for sequentially segmenting species. In contrast, progressive segmentation involves anterior‐posterior addition of gene expression stripes that do not originate in a SAZ and so far has only been described in long‐germ insects (Taylor & Dearden, 2021). This term was recently introduced to describe segmentation in the anterior of the jewel wasp ( Nasonia vitripennis ), which utilizes a dual mode in which distinct segmentation modes operate in different body regions (Rosenberg et al, 2014).…”

“…In Drosophila , this gene is expressed broadly across the whole trunk, overlaying completed pair‐rule patterns and prompting a simultaneous transition to segment polarity stripe patterns. The different spatial‐temporal deployment of opa and other timing factor genes in other insects led to the suggestion that opa serves as a “timing factor” throughout insects, potentially explaining heterochronic shifts in segmentation modes (Clark & Peel, 2018; Taylor & Dearden, 2021). Both the “Timing Factor” model and the Speed Regulation model also implicate posterior‐anterior gradients of caudal (cad) and Wnt signaling in the evolution of segmentation modes (Clark et al, 2019; Zhu et al, 2017).…”