Tergal and pleural wing-related tissues in the German cockroach and their implication to the evolutionary origin of insect wings.
Blattella germanica
Hox
evolutionary origin
insect wings
morphological novelty
serial homology
vestigial
Journal
Evolution & development
ISSN: 1525-142X
Titre abrégé: Evol Dev
Pays: United States
ID NLM: 100883432
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
06
11
2019
revised:
24
12
2020
accepted:
03
01
2021
pubmed:
28
1
2021
medline:
29
1
2022
entrez:
27
1
2021
Statut:
ppublish
Résumé
The acquisition of wings has facilitated the massive evolutionary success of pterygotes (winged insects), which now make up nearly three-quarters of described metazoans. However, our understanding of how this crucial structure has evolved remains quite elusive. Historically, two ideas have dominated in the wing origin debate, one placing the origin in the dorsal body wall (tergum) and the other in the lateral pleural plates and the branching structures associated with these plates. Through studying wing-related tissues in the wingless segments (such as wing serial homologs) of the beetle, Tribolium castaneum, we obtained several crucial pieces of evidence that support a third idea, the dual origin hypothesis, which proposes that wings evolved from a combination of tergal and pleural tissues. Here, we extended our analysis outside of the beetle lineage and sought to identify wing-related tissues from the wingless segments of the cockroach, Blattella germanica. Through detailed functional and expression analyses for a critical wing gene, vestigial (vg), along with re-evaluating the homeotic transformation of a wingless segment induced by an improved RNA interference protocol, we demonstrate that B. germanica possesses two distinct tissues in their wingless segments, one with tergal and one with pleural nature, that might be evolutionarily related to wings. This outcome appears to parallel the reports from other insects, which may further support a dual origin of insect wings. However, we also identified a vg-independent tissue that contributes to wing formation upon homeotic transformation, as well as vg-dependent tissues that do not appear to participate in wing formation, in B. germanica, indicating a more complex evolutionary history of the tissues that contributed to the emergence of insect wings.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
100-116Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Almudi, I., Vizueta, J., Wyatt, C. D. R., de Mendoza, A., Marlétaz, F., Firbas, P. N., Feuda, R., Masiero, G., Medina, P., Alcaina-Caro, A., Cruz, F., Gómez-Garrido, J., Gut, M., Alioto, T. S., Vargas-Chavez, C., Davie, K., Misof, B., González, J., Aerts, S., … Casares, F. (2020). Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings. Nature Communications, 11, 2631.
Angelini, D. R., & Kaufman, T. C. (2005). Comparative developmental genetics and the evolution of arthropod body plans. Annual Review of Genetics, 39, 95-119.
Averof, M., & Cohen, S. M. (1997). Evolutionary origin of insect wings from ancestral gills. Nature, 385, 627-630.
Azpiazu, N., & Morata, G. (2000). Function and regulation of homothorax in the wing imaginal disc of Drosophila. Development, 127, 2685-2693.
Baena-López, L. A., & García-Bellido, A. (2003). Genetic requirements of vestigial in the regulation of Drosophila wing development. Development, 130, 197-208.
Bernard, F., Lalouette, A., Gullaud, M., Jeantet, A. Y., Cossard, R., Zider, A., Ferveur, J. F., & Silber, J. (2003). Control of apterous by vestigial drives indirect flight muscle development in Drosophila. Developmental Biology, 260, 391-403.
Bruce, H. S., & Patel, N. H. (2020). Knockout of crustacean leg patterning genes suggests that insect wings and body walls evolved from ancient leg segments. Nature Ecology and Evolution, 4, 1703-1712.
Cifuentes, F. J., & Garcia-Bellido, A. (1997). Proximo-distal specification in the wing disc of Drosophila by the nubbin gene. Proceedings of the National Academy of Sciences of the United States of America, 94, 11405-11410.
Clark-Hachtel, C. M., Linz, D. M., & Tomoyasu, Y. (2013). Insights into insect wing origin provided by functional analysis of vestigial in the red flour beetle, Tribolium castaneum. Proceedings of the National Academy of Sciences of the United States of America, 110, 16951-16956.
Clark-Hachtel, C. M., Moe, M. R., & Tomoyasu, Y. (2018). Detailed analysis of the prothoracic tissues transforming into wings in the Cephalothorax mutants of Tribolium. Arthropod Structure & Development, 47, 352-361.
Clark-Hachtel, C. M., & Tomoyasu, Y. (2016). Exploring the origin of insect wings from an evo-devo perspective. Current Opinion in Insect Science, 13, 77-85.
Clark-Hachtel, C. M., & Tomoyasu, Y. (2020). Two sets of candidate crustacean wing homologues and their implication for the origin of insect wings. Nature Ecology and Evolution, 4, 1694-1702.
Deng, H., Bell, J. B., & Simmonds, A. J. (2010). Vestigial is required during late-stage muscle differentiation in Drosophila melanogaster embryos. Molecular Biology of the Cell, 21, 3304-3316.
Deng, H., Hughes, S. C., Bell, J. B., & Simmonds, A. J. (2009). Alternative requirements for Vestigial, Scalloped, and Dmef2 during muscle differentiation in Drosophila melanogaster. Molecular Biology of the Cell, 20, 256-269.
Elias-Neto, M., & Belles, X. (2016). Tergal and pleural structures contribute to the formation of ectopic prothoracic wings in cockroaches. Royal Society Open Science, 3, 160347.
Guthrie, D. M., & Tindall, A. R. (1968). The exoskeleton, The biology of the cockroach (pp. 23-60). Edward Arnold Publisher.
Halder, G., Polaczyk, P., Kraus, M. E., Hudson, A., Kim, J., Laughon, A., & Carroll, S. (1998). The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila. Genes and Development, 12, 3900-3909.
Hrycaj, S., Chesebro, J., & Popadić, A. (2010). Functional analysis of Scr during embryonic and post-embryonic development in the cockroach, Periplaneta americana. Developmental Biology, 341, 324-334.
Hu, Y., Schmitt-Engel, C., Schwirz, J., Stroehlein, N., Richter, T., Majumdar, U., & Bucher, G. (2018). A morphological novelty evolved by co-option of a reduced gene regulatory network and gene recruitment in a beetle. Proceedings of the Royal Society B: Biological Sciences, 285, 20181373.
Hughes, C. L., & Kaufman, T. C. (2002). Hox genes and the evolution of the arthropod body plan. Evolution & Development, 4, 459-499.
Kim, J., Sebring, A., Esch, J. J., Kraus, M. E., Vorwerk, K., Magee, J., & Carroll, S. B. (1996). Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature, 382, 133-138.
Kukalova-Peck, J. (1983). Origin of the insect wing and wing articulation from the arthropodan leg. Canadian Journal of Zoology, 61, 1618-1669.
Linz, D. M., Clark-Hachtel, C. M., Borràs-Castells, F., & Tomoyasu, Y. (2014). Larval RNA interference in the red flour beetle, Tribolium castaneum. Journal of Visualized Experiments, e52059.
Linz, D. M., & Tomoyasu, Y. (2018). Dual evolutionary origin of insect wings supported by an investigation of the abdominal wing serial homologs in Tribolium. Proceedings of the National Academy of Sciences of the United States of America, 115, E658-E667.
Maestro, J. L., Pascual, N., Treiblmayr, K., Lozano, J., & Bellés, X. (2010). Juvenile hormone and allatostatins in the German cockroach embryo. Insect Biochemistry and Molecular Biology, 40, 660-665.
Mashimo, Y., & Machida, R. (2017). Embryological evidence substantiates the subcoxal theory on the origin of pleuron in insects. Scientific Reports, 7, 12597.
Medved, V., Marden, J. H., Fescemyer, H. W., Der, J. P., Liu, J., Mahfooz, N., & Popadić, A. (2015). Origin and diversification of wings: Insights from a neopteran insect. Proceedings of the National Academy of Sciences of the United States of America, 112, 15946-15951.
Nagaso, H., Murata, T., Day, N., & Yokoyama, K. K. (2001). Simultaneous detection of RNA and protein by in situ hybridization and immunological staining. Journal of Histochemistry and Cytochemistry, 49, 1177-1182.
Ng, M., Diaz-Benjumea, F. J., & Cohen, S. M. (1995). nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development, 121, 589-599.
Niwa, N., Akimoto-Kato, A., Niimi, T., Tojo, K., Machida, R., & Hayashi, S. (2010). Evolutionary origin of the insect wing via integration of two developmental modules. Evolution & Development, 12, 168-176.
Ohde, T., Yaginuma, T., & Niimi, T. (2013). Insect morphological diversification through the modification of wing serial homologs. Science, 340, 495-498.
Pearson, J. C., Lemons, D., & McGinnis, W. (2005). Modulating Hox gene functions during animal body patterning. Nature Reviews Genetics, 6, 893-904.
Philip, B. N., & Tomoyasu, Y. (2011). Gene knockdown analysis by double-stranded RNA injection. Methods in Molecular Biology, 772, 471-497.
Piulachs, M. D., Pagone, V., & Bellés, X. (2010). Key roles of the Broad-Complex gene in insect embryogenesis. Insect Biochemistry and Molecular Biology, 40, 468-475.
Prokop, J., Pecharová, M., Nel, A., Hörnschemeyer, T., Krzemińska, E., Krzemiński, W., & Engel, M. S. (2017). Paleozoic nymphal wing pads support dual model of insect wing origins. Current Biology, 27, 263-269.
Quartau, J. A. (1986). An overview of the paranotal theory on the origin of the insect wings. Publicações do Instituto de Zoologia “Dr. Augusto Nobre” Fac. Ciencias Do Porto, 194, 1-42.
Rasnitsyn, A. P. (1981). A modified paranotal theory of insect wing origin. Journal of Morphology, 168, 331-338.
Requena, D., Álvarez, J. A., Gabilondo, H., Loker, R., Mann, R. S., & Estella, C. (2017). Origins and specification of the Drosophila wing. Current Biology, 27, 3826-3836.e5.
Rogers, B. T., Peterson, M. D., & Kaufman, T. C. (1997). Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern. Development, 124, 149-157.
Ross, M. H. (1964). Pronotal wings in Blattella germanica (L.) and their possible evolutionary significance. American Midland Naturalist, 71, 161-180.
Shippy, T. D., Coleman, C. M., Tomoyasu, Y., & Brown, S. J. (2009). Concurrent in situ hybridization and antibody staining in red flour beetle (Tribolium) embryos. Cold Spring Harbor Protocols, 4, pdb.prot5257.
Smith, F. W., & Jockusch, E. L. (2020). Into the body wall and back out again. Nature Ecology and Evolution, 4, 1580-1581.
Snodgrass, R. E. (1935a). The abdomen, Principles of insect morphology (pp. 246-279). Cornell University Press.
Snodgrass, R. E. (1935b). The thorax, Principles of insect morphology (pp. 157-192). Cornell University Press.
Sánchez-Higueras, C., Sotillos, S., & Castelli-Gair Hombría, J. (2014). Common origin of insect trachea and endocrine organs from a segmentally repeated precursor. Current Biology, 24, 76-81.
Tanaka, A., & Ito, T. (1997). Studies of the genetics and expression of Prowing (Pw): A primitive homeotic mutant of the German cockroach, Blattella germanica. Zoological Science, 14, 339-346.
Tomoyasu, Y. (2018). Evo-devo: The double identity of insect wings. Current Biology, 28, R75-R77.
Tomoyasu, Y., Arakane, Y., Kramer, K. J., & Denell, R. E. (2009). Repeated co-options of exoskeleton formation during wing-to-elytron evolution in beetles. Current Biology, 19, 2057-2065.
Tomoyasu, Y., Ohde, T., & Clark-Hachtel, C. M. (2017). What serial homologs can tell us about the origin of insect wings. F1000Research, 6, 268.
Tomoyasu, Y., Wheeler, S. R., & Denell, R. E. (2005). Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature, 433, 643-647.
Williams, J. A., Bell, J. B., & Carroll, S. B. (1991). Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes and Development, 5, 2481-2495.