Insect wings and body wall evolved from ancient leg segments
Preprint posted on January 31, 2018 https://www.biorxiv.org/content/early/2018/01/31/244541
Article now published in Nature Ecology & Evolution at http://dx.doi.org/10.1038/s41559-020-01349-0
Two sets of wing homologs in the crustacean, Parhyale hawaiensis
Preprint posted on December 18, 2017 https://www.biorxiv.org/content/early/2017/12/18/236281
Article now published in Nature Ecology & Evolution at http://dx.doi.org/10.1038/s41559-020-1257-8
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 ClarkCategories: developmental biology, evolutionary biology, genetics
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.
Posted on: 7th February 2018 , updated on: 19th February 2018
Have your say
Sign up to customise the site to your preferences and to receive alerts
Register hereAlso in the developmental biology category:
Maintenance of neurotransmitter identity by Hox proteins through a homeostatic mechanism
Selected by | Chee Kiang Ewe |
1
FGF signaling promotes precursor spreading for adult adipogenesis in Drosophila
Selected by | Anastasia Moraiti |
1
Cell Rearrangement Generates Pattern Emergence as a Function of Temporal Morphogen Exposure
Selected by | Andrew Montequin |
1
Also in the evolutionary biology category:
Combinatorial interactions of Hox genes establish appendage diversity of the amphipod crustacean Parhyale hawaiensis
AND
Distinct regulation of Hox genes by Polycomb Group genes in a crustacean
Selected by | Olivia Tidswell |
2
The Hox gene Antennapedia regulates wing development through 20-hydroxyecdysone in insect
Selected by | Lisa Hanna |
Annelid functional genomics reveal the origins of bilaterian life cycles
Selected by | Paul Bump |
1
Also in the genetics category:
Maintenance of neurotransmitter identity by Hox proteins through a homeostatic mechanism
Selected by | Chee Kiang Ewe |
1
Long read mitochondrial genome sequencing using Cas9-guided adaptor ligation
Selected by | Nate Mullin |
Increased gene dosage and mRNA expression from chromosomal duplications in C. elegans
Selected by | Chee Kiang Ewe |
1
preListsdevelopmental biology category:
in the2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
List by | Nándor Lipták |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
List by | Osvaldo Contreras |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
List by | Alex Eve |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
List by | Jesus Victorino |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
List by | Alex Eve |
Society for Developmental Biology 79th Annual Meeting
Preprints at SDB 2020
List by | Irepan Salvador-Martinez, Martin Estermann |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
List by | Ana Dorrego-Rivas |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
List by | Ana Dorrego-Rivas |
Cell Polarity
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
List by | Yamini Ravichandran |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
List by | Maiko Kitaoka et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
List by | Paul Gerald L. Sanchez and Stefano Vianello |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
List by | Madhuja Samaddar et al. |
EDBC Alicante 2019
Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.
List by | Sergio Menchero et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
List by | Dey Lab |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
List by | Alex Eve |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
List by | Rob Hynds |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
List by | Alexa Sadier |
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
List by | Dey Lab |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
List by | Shikha Nayar |
Also in the evolutionary biology category:
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
List by | Alex Eve |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
List by | Ana Dorrego-Rivas |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
List by | Hiral Shah |
COVID-19 / SARS-CoV-2 preprints
List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic
List by | Dey Lab, Zhang-He Goh |
1
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
List by | Alexa Sadier |
Also in the genetics category:
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
List by | Nándor Lipták |
2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
List by | Nándor Lipták |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
List by | Jesus Victorino |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
List by | Hiral Shah |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
List by | Sandra Malmgren Hill |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
List by | Shikha Nayar |
4 years
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?!