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Miniaturization re-establishes symmetry in the wing folding patterns of featherwing beetles

ABSTRACT: Most microinsects have feather-like bristled wings, a state known as ptiloptery, but featherwing beetles (family Ptiliidae) are unique among winged microinsects in their ability to fold such wings. An asymmetrical wing folding pattern, found also in the phylogenetically related rove beetles (Staphylinidae), was ancestral for Ptiliidae. Using scanning electron, confocal laser scanning, and optical microscopy, high-speed video recording, and 3D reconstruction, we analyze in detail the symmetrical wing folding pattern and the mechanism of the folding and unfolding of the wings in Acrotrichis sericans (Coleoptera: Ptiliidae) and show how some of the smaller featherwing beetles have reverted to strict symmetry in their wing folding. The wings are folded in three phases by bending along four lines (with the help of wing folding patches on the abdominal tergites) and locked under the closed elytra; they unfold passively in two phases, apparently with the help of the elasticity provided by resilin unevenly distributed in the wing and of convexities forming in the cross-sections of the unfolding wing, making it stiffer. The minimum duration of folding is 3.5 s; unfolding is much more rapid (minimum duration lowest recorded in beetles, 0.038 s). The folding ratio of A. sericans is 3.31 (without setae), which is greater than in any beetle in which it has been measured. The symmetrical wing folding pattern found in A. sericans and in all of the smallest ptiliids, in which ptiloptery is especially pronounced, is the only known example of symmetry re-established during miniaturization. This direction of evolution is remarkable because miniaturization is known to result in various asymmetries, while in this case miniaturization was accompanied by reversal to symmetry, probably associated with the evolution of ptiloptery. Our results on the pattern and mechanisms of wing folding and unfolding can be used in robotics for developing miniature biomimetic robots: the mechanisms of wing folding and unfolding in Ptiliidae present a challenge to engineers who currently work at designing ever smaller flying robots and may eventually produce miniature robots with foldable wings.

SUBMITTER: Petrov P

PROVIDER: S-EPMC7536412 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Project description:This study examines the evolution hindwing shape in Chinese dung beetle species using morphometric and phylogenetic analyses. Previous studies have analyzed the evolution of wing shape within a single or very few species, or by comparing only a few wing traits. No study has analyzed wing shape evolution of a large number of species, or quantitatively compared morphological variation of wings with proposed phylogenetic relationships. This study examines the morphological variation of hindwings based on 19 landmarks, 119 morphological characters, and 81 beetle species. Only one most parsimonious tree (MPT) was found based on 119 wing and body characters. To better understand the possible role of the hindwing in the evolution of Scarabaeinae, additional phylogenetic analyses were proposed based on the only body features (106 characters, wing characters excluded). Two MPT were found based on 106 body characters, and five nodes were collapsed in a strict consensus. There was a strong correlation between the morphometric tree and all phylogenetic trees (r>0.5). Reconstructions of the ancestral wing forms suggest that Scarabaeinae hindwing morphology has not changed substantially over time, but the morphological changes that do occur are focused at the base of the wing. These results suggest that flight has been important since the origin of Scarabaeinae, and that variation in hindwing morphology has been limited by functional constraints. Comparison of metric disparity values and relative evolutionary sequences among Scarabaeinae tribes suggest that the primitive dung beetles had relatively diverse hindwing morphologies, while advanced dung beetles have relatively similar wing morphologies. The strong correlation between the morphometric tree and phylogenetic trees suggest that hindwing features reflect the evolution of whole body morphology and that wing characters are suitable for the phylogenetic analyses. By integrating morphometric and cladistic approaches, this paper sheds new light on the evolution of dung beetle hind wings.

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Miniaturization re-establishes symmetry in the wing folding patterns of featherwing beetles

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