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A simple developmental model recapitulates complex insect wing venation patterns.

ABSTRACT: Insect wings are typically supported by thickened struts called veins. These veins form diverse geometric patterns across insects. For many insect species, even the left and right wings from the same individual have veins with unique topological arrangements, and little is known about how these patterns form. We present a large-scale quantitative study of the fingerprint-like "secondary veins." We compile a dataset of wings from 232 species and 17 families from the order Odonata (dragonflies and damselflies), a group with particularly elaborate vein patterns. We characterize the geometric arrangements of veins and develop a simple model of secondary vein patterning. We show that our model is capable of recapitulating the vein geometries of species from other, distantly related winged insect clades.

SUBMITTER: Hoffmann J

PROVIDER: S-EPMC6176563 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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A simple developmental model recapitulates complex insect wing venation patterns.

Hoffmann Jordan J Donoughe Seth S Li Kathy K Salcedo Mary K MK Rycroft Chris H CH

Proceedings of the National Academy of Sciences of the United States of America 20180917 40

Insect wings are typically supported by thickened struts called veins. These veins form diverse geometric patterns across insects. For many insect species, even the left and right wings from the same individual have veins with unique topological arrangements, and little is known about how these patterns form. We present a large-scale quantitative study of the fingerprint-like "secondary veins." We compile a dataset of wings from 232 species and 17 families from the order Odonata (dragonflies and ...[more]

PMID: 30224459

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Project description:Dragonflies and damselflies, belonging to the order Odonata, are known to be excellent fliers with versatile flight capabilities. The ability to fly over a wide range of speeds, high manoeuvrability and great agility are a few characteristics of their flight. The architecture of the wings and their structural elements have been found to play a major role in this regard. However, the precise influence of individual wing components on the flight performance of these insects remains unknown. The design of the wing basis (so called basal complex) and the venation of this part are responsible for particular deformability and specific shape of the wing blade. However, the wing bases are rather different in representatives of different odonate groups. This presumably reflects the dimensions of the wings on one hand, and different flight characteristics on the other hand. In this article, we develop the first three-dimensional (3D) finite element (FE) models of the proximal part of the wings of typical representatives of five dragonflies and damselflies families. Using a combination of the basic material properties of insect cuticle, a linear elastic material model and a nonlinear geometric analysis, we simulate the mechanical behaviour of the wing bases. The results reveal that although both the basal venation and the basal complex influence the structural stiffness of the wings, it is only the latter which significantly affects their deformation patterns. The use of numerical simulations enabled us to address the role of various wing components such as the arculus, discoidal cell and triangle on the camber formation in flight. Our study further provides a detailed representation of the stress concentration in the models. The numerical analysis presented in this study is not only of importance for understanding structure-function relationship of insect wings, but also might help to improve the design of the wings for biomimetic micro-air vehicles (MAVs).

Project description:The last time the phylogenetic relationships among members of the family Hemerobiidae were studied quantitatively was over 12 years ago and based exclusively on morphology. Our study builds upon this morphological evidence by adding sequence data from three gene loci to provide a total evidence phylogeny of brown lacewings (Neuroptera: Hemerobiidae). Thirty-seven species representing nineteen Hemerobiidae genera were compared with outgroups from the families Ithonidae, Psychopsidae and Chrysopidae in Bayesian and parsimony analyses using a single nuclear gene (CAD) and two mitochondrial (16S rDNA and Cytochrome Oxidase I) genes. We compare divergence time estimates of Hemerobiidae cladogenesis under the two most commonly used relaxed clock models and discuss the evolution of wing venation in the family.We recovered a phylogeny largely incongruent with previously published morphological studies, although all but two subfamilies (i.e., Notiobiellinae and Drepanacrinae) were recovered as monophyletic. We found the subfamily Drepanacrinae paraphyletic with respect to Psychobiellinae, and Notiobiellinae to be polyphyletic. We thus offer a revised concept of Notiobiellinae, comprising only Notiobiella Banks, and erect a new subfamily Zachobiellinae including the remaining genera previously placed in Notiobiellinae. Psychobiellinae is synonymized with Drepanacrinae. Unlike the previous hypothesis that proposed a remarkably laddered topology, our tree suggests that hemerobiids diverged as three main clades. Moreover, in contrast to the vein proliferation hypothesis, we found that hemerobiids have instead undergone multiple reductions in the number of radial veins, this scenario questions the relevance of this character as diagnostic of various subfamiliesOur phylogenetic hypothesis and divergence times analysis suggest that extant hemerobiids originated around the end of the Triassic and evolved as three distinct clades that diverged from one another during the Late Jurassic to Early Cretaceous. Contrary to earlier phylogenetic hypotheses, Carobius Banks (Carobiinae) is sister to the previously unplaced genus Notherobius New in a clade more closely related to Sympherobiinae, Megalominae and Zachobiellinae subfam. nov. The addition of taxa which are not available for DNA sequencing should be the focus of future studies, especially Adelphohemerobius Oswald, which is particularly important to test our inferences regarding the evolution of wing venation in Hemerobiidae.

Project description:Insect wings show a high variability in wing venation. Selection for function, developmental pathways and phylogeny likely influenced wing vein diversification, however, quantitative data to estimate these influences and their interplay are missing. Here, it is tested how dragonfly wing vein configuration is influenced by functional demands, development, phylogeny and allometry using the concepts of modularity and integration. In an evolutionary context, modules are sets of characters that evolve in relative independence to other characters, while integration refers to a high degree of association between subparts of a structure. Results show allometric and phylogenetic signal in the wing shape variation, however, patterns of integration and modularity are not influenced by these two factors. Overall, dragonfly wings are highly integrated structures with almost no modular signal. Configuration changes in one wing vein or wing area thus influence wing shape as a whole. Moreover, the fore- and hindwings correlate with each other in their evolutionary shape variation supporting biomechanical data of wing interdependence. Despite the overall high degree of evolutionary integration, functional hypotheses of modularity could be confirmed for two wing areas, the arculus-triangle complex at the base of the wing which is responsible for passive wing folding especially during flapping flight and the location of the pterostigma, a coloured wing cell which is more heavy that other wing cells and passively regulates wing pitch as well as critical flight speeds during gliding. Although evolving as distinct modules, these specific vein regions also show high integration and evolve at the same rates like the whole wing which suggests an influence of these structures on the shape evolution of the rest of the wing. Their biomechanical role as passive regulators of wing corrugation and wing pitch suggests that these structures decisively influenced the evolution of advanced modern flight styles and explains their retention once they had evolved early within the lineage Odonatoptera.

Dataset Information

A simple developmental model recapitulates complex insect wing venation patterns.

Publications

A simple developmental model recapitulates complex insect wing venation patterns.

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