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

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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.

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          Most cited references53

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          Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data

          Summary: The two main functions of bioinformatics are the organization and analysis of biological data using computational resources. Geneious Basic has been designed to be an easy-to-use and flexible desktop software application framework for the organization and analysis of biological data, with a focus on molecular sequences and related data types. It integrates numerous industry-standard discovery analysis tools, with interactive visualizations to generate publication-ready images. One key contribution to researchers in the life sciences is the Geneious public application programming interface (API) that affords the ability to leverage the existing framework of the Geneious Basic software platform for virtually unlimited extension and customization. The result is an increase in the speed and quality of development of computation tools for the life sciences, due to the functionality and graphical user interface available to the developer through the public API. Geneious Basic represents an ideal platform for the bioinformatics community to leverage existing components and to integrate their own specific requirements for the discovery, analysis and visualization of biological data. Availability and implementation: Binaries and public API freely available for download at http://www.geneious.com/basic, implemented in Java and supported on Linux, Apple OSX and MS Windows. The software is also available from the Bio-Linux package repository at http://nebc.nerc.ac.uk/news/geneiousonbl. Contact: peter@biomatters.com
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            Mutations affecting segment number and polarity in Drosophila.

            In systematic searches for embryonic lethal mutants of Drosophila melanogaster we have identified 15 loci which when mutated alter the segmental pattern of the larva. These loci probably represent the majority of such genes in Drosophila. The phenotypes of the mutant embryos indicate that the process of segmentation involves at least three levels of spatial organization: the entire egg as developmental unit, a repeat unit with the length of two segments, and the individual segment.
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              The developmental genetics of homology.

              P. Wagner (2007)
              Homology is an essential idea of biology, referring to the historical continuity of characters, but it is also conceptually highly elusive. The main difficulty is the apparently loose relationship between morphological characters and their genetic basis. Here I propose that it is the historical continuity of gene regulatory networks rather than the expression of individual homologous genes that underlies the homology of morphological characters. These networks, here referred to as 'character identity networks', enable the execution of a character-specific developmental programme.
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                Author and article information

                Contributors
                Journal
                Front Cell Dev Biol
                Front Cell Dev Biol
                Front. Cell Dev. Biol.
                Frontiers in Cell and Developmental Biology
                Frontiers Media S.A.
                2296-634X
                06 August 2021
                2021
                : 9
                : 695135
                Affiliations
                Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem , Jerusalem, Israel
                Author notes

                Edited by: Alessandro Minelli, University of Padua, Italy

                Reviewed by: Aleksandar Popadic, Wayne State University, United States; Bruno Cossermelli Vellutini, Max Planck Institute of Molecular Cell Biology and Genetics, Max Planck Society (MPG), Germany

                *Correspondence: Ariel D. Chipman, ariel.chipman@ 123456huji.ac.il

                This article was submitted to Evolutionary Developmental Biology, a section of the journal Frontiers in Cell and Developmental Biology

                Article
                10.3389/fcell.2021.695135
                8378449
                34422818
                6d983250-9069-4a68-b09b-24175e89601c
                Copyright © 2021 Lev and Chipman.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 14 April 2021
                : 19 July 2021
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 53, Pages: 10, Words: 0
                Funding
                Funded by: Israel Science Foundation 10.13039/501100003977
                Categories
                Cell and Developmental Biology
                Original Research

                insect,arthropod,evolution,segmentation,evo-devo,head,grn evolution,gene network analysis

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