Menu

Close

Insect wings and body wall evolved from ancient leg segments

Heather S Bruce, Nipam H Patel

Preprint posted on January 31, 2018 https://www.biorxiv.org/content/early/2018/01/31/244541

and

Two sets of wing homologs in the crustacean, Parhyale hawaiensis

Courtney M Clark-Hachtel, Yoshinori Tomoyasu

Preprint posted on December 18, 2017 https://www.biorxiv.org/content/early/2017/12/18/236281

How did insects get their wings? Two preprints use CRISPR/Cas9 knockdown approaches in a crustacean to shed light on this hitherto controversial question.

Selected by Erik Clark

Background

The invention of insect flight 350 million years ago was momentous for the history of life on earth. However, the evolutionary origin of insect wings has been debated, unresolved, for over a century. Were they outgrowths of the insect body wall, were they exaptations of crustacean “epipods” (projections from proximal leg segments, including structures such as gills), or were they formed from a merger of the two?

Model organism studies don’t help us much, because the way that Drosophila makes its wings (from imaginal discs) is extremely derived.  In recent years, however, studies in other insects have lent strong support to the “dual origin” hypothesis: in segments lacking wings, two separate tissues (the dorsal body wall and the pleural plates) express “wing” genes, and both contribute to ectopic wings formed in Hox gene knockdowns. However, it still hasn’t been clear whether these tissues ancestrally expressed wing genes, or simply co-opted them.

 

Key findings

Now, a pair of CRISPR/Cas9 studies in the amphipod crustacean, Paryhale hawaiensis, provide us with some clear-cut answers. Clark-Hachtel and Tomoyasu show that wing genes are necessary for the development of the dorsal body wall and epipods in Parhyale, demonstrating that the presence of a “wing” gene regulatory network (GRN) in these structures long predates the evolution of wings themselves.

In turn, Bruce and Patel knock down a number of leg patterning genes and show not only that the most proximal epipod in Parhyale is homologous to the insect pleural plate, but also that the dorsal “body wall” of both Parhyale and insects is actually a cryptic proximal leg segment, still present in other groups of crustaceans. Therefore, the two tissues from which wings develop in insects are both derived from crustacean epipods, and their shared gene expression results not from co-option, but from their common inheritance of an ancestral “epipod” GRN.

 

My take

This proposal offers an elegant solution to the wing origin debate, accounting for much of the evidence in favour of each of the three rival hypotheses. I also appreciated the accessibility of the text, which sidesteps much of the confusing morphological jargon of the insect/crustacean fields in favour of simple, colour-coded diagrams, allowing an outsider like me to follow the arguments. Of course, much more work will be required before we will understand how and why recognisable wings evolved within hexapods from these proto-structures. But as to the sticky question of their homology – case closed?

 

Related Research

Linz DM, Tomoyasu Y. (2018) Dual evolutionary origin of insect wings supported by an investigation of the abdominal wing serial homologs in Tribolium. PNAS 115, E658-E667.

Prokob J, Pecharova M, Nel A, Hornschemeyer T, Krzeminska E, Krzeminski W, Engel MS. (2017). Paleozoic nymphal wing pads support dual model of insect wing origins. Current Biology, 27, 263-269.

Martin A, Serano JM, Jarvis E, Bruce HS, Wang J, Ray S, Barker CA, O’Connell LC, Patel NH. (2015). CRISPR/Cas9 mutagenesis reveals versatile roles of Hox genes in crustacean limb specification and evolution. Current Biology 26, 14-26.

Tags: evo-devo, evolution

(2 votes)




  • Authors' response

    Yoshi Tomoyasu and Courtney Clark-Hachtel shared about Two sets of wing homologs in the crustacean, Parhyale hawaiensis

    Yoshi on the significance of the findings:

    The two studies complement each other, and together I believe that they tell an intriguing story about how complex novel structures evolve, which will no doubt significantly influence the future direction of the debates on the origin of insect wings, as well as on the evolution of morphological novelty in general.

     

    Courtney’s “behind the paper” story:

    One of my favorite moments from this project was the first time that I observed a ‘wingless crustacean’. When I saw that both dorsal body wall and proximal leg tissues were affected by wing gene knock-out in Parhyale and realized that this seemed to support what we had been seeing in wingless segments of insects, I got so excited. As scientists, we live for these eureka moments that can be few and far between in our work, and this moment was definitely a defining eureka moment for this project.

    1 comment

    3 months

    Rafael Galupa

    Thanks Erik! A great example of how a specific GRN has been exploited throughout evolution… And probably a good model to keep deepening our understanding of the mechanisms behind that. I wonder how easy it is to manipulate this crustacean?!




    0

    Have your say

    Your email address will not be published. Required fields are marked *

    Sign up to customise the site to your preferences and to receive alerts

    Register here

    Also in the developmental biology category:

    Rearing temperature and fatty acid supplementation jointly affect membrane fluidity and heat tolerance in Daphnia

    Dominik Martin-Creuzburg, Bret L. Coggins, Dieter Ebert, et al.



    Selected by Alexander Little

    A SoxB gene acts as an anterior gap gene and regulates posterior segment addition in the spider Parasteatoda tepidariorum

    Christian L. B. Paese, Anna Schoenauer, Daniel J. Leite, et al.



    Selected by Erik Clark

    1

    Cell type-specific interchromosomal interactions as a mechanism for transcriptional diversity

    Adan Horta, Kevin Monahan, Lisa Bashkirova, et al.



    Selected by Boyan Bonev

    Germ layer specific regulation of cell polarity and adhesion gives insight into the evolution of mesoderm.

    Miguel Salinas-Saavedra, Amber Q. Rock, Mark Q. Martindale



    Selected by ClaireS & SophieM

    1

    Wnt/β-catenin regulates an ancient signaling network during zebrafish scale development

    Andrew J Aman, Alexis N Fulbright, David M Parichy



    Selected by Andreas van Impel

    Tissue flow induces cell shape changes during organogenesis

    Gonca Erdemci-Tandogan, Madeline J.Clark, Jeffrey D. Amack, et al.



    Selected by Jacky G. Goetz

    Temporal Control of Transcription by Zelda in living Drosophila embryos

    Jeremy Dufourt, Antonio Trullo, Jennifer Hunter, et al.



    Selected by Teresa Rayon

    1

    An atlas of silencer elements for the human and mouse genomes

    Naresh Doni Jayavelu, Ajay Jajodia, Arpit Mishra, et al.



    Selected by Rafael Galupa

    1

    Genetically regulated human NODAL splice variants are differentially post-transcriptionally processed and functionally distinct

    Scott D Findlay, Olena Bilyk, Kiefer Lypka, et al.



    Selected by Pierre Osteil

    RNA-directed activation of cytoplasmic dynein-1 in reconstituted transport RNPs

    Mark A McClintock, Carly I Dix, Christopher M Johnson, et al.

    AND

    Recruitment of Two Dyneins to an mRNA-Dependent Bicaudal D Transport Complex

    Thomas E. Sladewski, Neil Billington, M. Yusuf Ali, et al.



    Selected by Dmitry Nashchekin

    Long-range Notch-mediated tissue patterning requires actomyosin contractility

    Ginger Hunter, Li He, Norbert Perrimon, et al.



    Selected by Yara E. Sánchez Corrales

    PIN7 auxin carrier is a terminator of radial root expansion in Arabidopsis thaliana

    Michel Ruiz Rosquete, Jurgen Kleine-Vehn

    AND

    PILS6 is a temperature-sensitive regulator of nuclear auxin input and organ growth in Arabidopsis thaliana

    Elena Feraru, Mugurel I. I Feraru, Elke Barbez, et al.



    Selected by Erin Sparks

    Bioelectric-calcineurin signaling module regulates allometric growth and size of the zebrafish fin

    Jacob Daane, Jennifer Lanni, Ina Rothenberg, et al.



    Selected by Alberto Rosello-Diez

    1

    Long-term live imaging of the Drosophila adult midgut reveals real-time dynamics of cell division, differentiation, and loss

    Judy Martin, Erin Nicole Sanders, Paola Moreno-Roman, et al.



    Selected by Natalie Dye

    From spiral cleavage to bilateral symmetry: The developmental cell lineage of the annelid brain

    Pavel Vopalensky, Maria Antonietta Tosches, Kaia Achim, et al.



    Selected by Erik Clark

    A 3D model of human skeletal muscle innervated with stem cell-derived motor neurons enables epsilon-subunit targeted myasthenic syndrome studies

    Mohsen Afshar Bakooshli, Ethan S Lippmann, Ben Mulcahy, et al.



    Selected by Chris Demers

    Also in the evolutionary biology category:

    A SoxB gene acts as an anterior gap gene and regulates posterior segment addition in the spider Parasteatoda tepidariorum

    Christian L. B. Paese, Anna Schoenauer, Daniel J. Leite, et al.



    Selected by Erik Clark

    1

    Germ layer specific regulation of cell polarity and adhesion gives insight into the evolution of mesoderm.

    Miguel Salinas-Saavedra, Amber Q. Rock, Mark Q. Martindale



    Selected by ClaireS & SophieM

    1

    Wnt/β-catenin regulates an ancient signaling network during zebrafish scale development

    Andrew J Aman, Alexis N Fulbright, David M Parichy



    Selected by Andreas van Impel

    Bacteriophage cooperation suppresses CRISPR-Cas3 and Cas9 immunity

    Adair L Borges, Jenny Y Zhang, MaryClare Rollins, et al.

    AND

    Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity

    Mariann Landsberger, Sylvain Gandon, Sean Meaden, et al.



    Selected by Fillip Port

    Dynamic Kinetochore Size Regulation Promotes Microtubule Capture And Chromosome Biorientation In Mitosis

    Carlos Sacristan, Misbha Ahmad, Jenny Keller, et al.

    AND

    Self-assembly of the RZZ complex into filaments drives kinetochore expansion in the absence of microtubule attachment

    Cláudia Pereira, Rita M Reis, José B Gama, et al.



    Selected by Gautam Dey

    Individual- and population-level drivers of consistent foraging success across environments

    Lysanne Snijders, Ralf HJM Kurvers, Stefan Krause, et al.



    Selected by Rasmus Ern

    The ancestral animal genetic toolkit revealed by diverse choanoflagellate transcriptomes

    Daniel Richter, Parinaz Fozouni, Michael Eisen, et al.



    Selected by Rafael Galupa

    Genome-wide selection scans integrated with association mapping reveal mechanisms of physiological adaptation across a salinity gradient in killifish

    Reid S. Brennan, Timothy M. Healy, Heather J. Bryant, et al.



    Selected by Andy Turko

    From Armament to Ornament: Performance Trade-Offs in the Sexual Weaponry of Neotropical Electric Fishes

    Kory M. Evans, Maxwell J. Bernt, Matthew A. Kolmann, et al.



    Selected by Cassandra Donatelli

    Insect wings and body wall evolved from ancient leg segments

    Heather S Bruce, Nipam H Patel

    AND

    Two sets of wing homologs in the crustacean, Parhyale hawaiensis

    Courtney M Clark-Hachtel, Yoshinori Tomoyasu



    Selected by Erik Clark

    2

    Also in the genetics category:

    Cancer modeling by Transgene Electroporation in Adult Zebrafish (TEAZ)

    Scott J Callahan, Stephanie Tepan, Yan M Zhang, et al.



    Selected by Hannah Brunsdon

    PDX Finder: A Portal for Patient-Derived tumor Xenograft Model Discovery

    Nathalie Conte, Jeremy Mason, Csaba Halmagyi, et al.



    Selected by Carmen Adriaens

    Bioelectric-calcineurin signaling module regulates allometric growth and size of the zebrafish fin

    Jacob Daane, Jennifer Lanni, Ina Rothenberg, et al.



    Selected by Alberto Rosello-Diez

    1

    Long-term live imaging of the Drosophila adult midgut reveals real-time dynamics of cell division, differentiation, and loss

    Judy Martin, Erin Nicole Sanders, Paola Moreno-Roman, et al.



    Selected by Natalie Dye

    F-actin patches nucleated on chromosomes coordinate capture by microtubules in oocyte meiosis

    Mariia Burdyniuk, Andrea Callegari, Masashi Mori, et al.



    Selected by Binyam Mogessie

    Comprehensive characterization of transcript diversity at the human NODAL locus

    Scott D Findlay, Lynne-Marie Postovit



    Selected by Christian Ramos

    Cell-nonautonomous local and systemic responses to cell arrest enable long-bone catch-up growth

    Alberto Rosello-Diez, Linda Madisen, Sebastien Bastide, et al.



    Selected by Natalie Dye

    Precise temporal regulation of alternative splicing during neural development

    Sebastien M Weyn-Vanhentenryck, Huijuan Feng, Dmytro Ustianenko, et al.



    Selected by James Gagnon

    Mutations in Bcl9 and Pygo genes cause congenital heart defects by tissue-specific perturbation of Wnt/β-catenin signaling

    Claudio Cantù, Anastasia Felker, Dario Zimmerli, et al.



    Selected by Andreas van Impel
    Close

    We want to make our website, and the services we provide, useful and reliable. This sometimes involves placing small amounts of information called cookies on the device you used to access the internet. If you continue to use this website we will assume you are happy to accept our cookies.

    Accept