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      Anatomy of adult Megaphragma (Hymenoptera: Trichogrammatidae), one of the smallest insects, and new insight into insect miniaturization

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          Abstract

          The body size, especially in cases of extreme reduction, is an important characteristic that strongly determines the morphology, physiology, and biology of animals. Miniaturization is a widespread trend in animal evolution and one of the principal directions of evolution in insects. Miniaturization-related features of insect morphology have been subject to intensive studies during the last few years, but the structure of the smallest insects remains insufficiently known. It is especially important to study hymenopterans of the genus Megaphragma, which include the smallest flying insects and a species in which an almost anucleate nervous system was recently discovered. This article is the first detailed study of the external and internal morphology of adults of Megaphragma mymaripenne and M. amalphitanum using histological methods, 3D computer modeling and other techniques. It is shown that in spite of the extremely small size the organization of Megaphragma retains a considerkable level of structural complexity. On the other hand, miniaturization leads to re-organizations of several organ systems. Unique structural features related to miniaturization have been found in both species: lysis of cell bodies and nuclei of neurons at late stages of pupal development, absence of the heart, and considerable reductions in the set of muscles. Comparative analysis of structure in the smallest insects representing different taxa has revealed common features of the evolutionary process of miniaturization in insects.

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          Most cited references40

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          A Gross Anatomy Ontology for Hymenoptera

          Hymenoptera is an extraordinarily diverse lineage, both in terms of species numbers and morphotypes, that includes sawflies, bees, wasps, and ants. These organisms serve critical roles as herbivores, predators, parasitoids, and pollinators, with several species functioning as models for agricultural, behavioral, and genomic research. The collective anatomical knowledge of these insects, however, has been described or referred to by labels derived from numerous, partially overlapping lexicons. The resulting corpus of information—millions of statements about hymenopteran phenotypes—remains inaccessible due to language discrepancies. The Hymenoptera Anatomy Ontology (HAO) was developed to surmount this challenge and to aid future communication related to hymenopteran anatomy. The HAO was built using newly developed interfaces within mx, a Web-based, open source software package, that enables collaborators to simultaneously contribute to an ontology. Over twenty people contributed to the development of this ontology by adding terms, genus differentia, references, images, relationships, and annotations. The database interface returns an Open Biomedical Ontology (OBO) formatted version of the ontology and includes mechanisms for extracting candidate data and for publishing a searchable ontology to the Web. The application tools are subject-agnostic and may be used by others initiating and developing ontologies. The present core HAO data constitute 2,111 concepts, 6,977 terms (labels for concepts), 3,152 relations, 4,361 sensus (links between terms, concepts, and references) and over 6,000 text and graphical annotations. The HAO is rooted with the Common Anatomy Reference Ontology (CARO), in order to facilitate interoperability with and future alignment to other anatomy ontologies, and is available through the OBO Foundry ontology repository and BioPortal. The HAO provides a foundation through which connections between genomic, evolutionary developmental biology, phylogenetic, taxonomic, and morphological research can be actualized. Inherent mechanisms for feedback and content delivery demonstrate the effectiveness of remote, collaborative ontology development and facilitate future refinement of the HAO.
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            Small is beautiful: features of the smallest insects and limits to miniaturization.

            Miniaturization leads to considerable reorganization of structures in insects, affecting almost all organs and tissues. In the smallest insects, comparable in size to unicellular organisms, modifications arise not only at the level of organs, but also at the cellular level. Miniaturization is accompanied by allometric changes in many organ systems. The consequences of miniaturization displayed by different insect taxa include both common and unique changes. Because the smallest insects are among the smallest metazoans and have the most complex organization among organisms of the same size, their peculiar structural features and the factors that limit their miniaturization are of considerable theoretical interest to general biology.
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              The scaling and allometry of organ size associated with miniaturization in insects: A case study for Coleoptera and Hymenoptera

              The study of the influence of body size on structure in animals, as well as scaling of organs, is one of the key areas of functional and evolutionary morphology of organisms. Most studies in this area treated mammals or birds; comparatively few studies are available on other groups of animals. Insects, because of the huge range of their body sizes and because of their colossal diversity, should be included in the discussion of the problem of scaling and allometry in animals, but to date they remain insufficiently studied. In this study, а total of 28 complete (for all organs) and 24 partial 3D computer reconstructions of body and organs have been made for 23 insect species of 11 families and five orders. The relative volume of organs was analyzed based on these models. Most insect organs display a huge potential for scaling and for retaining their organization and constant relative volume. By contrast, the relative volume of the reproductive and nervous systems increases by a considerable factor as body size decreases. These systems can geometrically restrain miniaturization in insects and determine the limits to the smallest possible body size.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 May 2017
                2017
                : 12
                : 5
                : e0175566
                Affiliations
                [001]Department of Entomology, Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia
                Smithsonian National Museum of Natural History, UNITED STATES
                Author notes

                Competing Interests: The author has declared that no competing interests exist.

                • Conceptualization: AAP.

                • Data curation: AAP.

                • Formal analysis: AAP.

                • Funding acquisition: AAP.

                • Investigation: AAP.

                • Methodology: AAP.

                • Project administration: AAP.

                • Validation: AAP.

                • Visualization: AAP.

                • Writing – original draft: AAP.

                • Writing – review & editing: AAP.

                Author information
                http://orcid.org/0000-0002-6214-3627
                Article
                PONE-D-16-42043
                10.1371/journal.pone.0175566
                5414980
                28467417
                5c45377a-8509-464d-962c-b1cb54732553
                © 2017 Alexey A. Polilov

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 October 2016
                : 28 March 2017
                Page count
                Figures: 9, Tables: 0, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100006769, Russian Science Foundation;
                Award ID: 14-14-00208
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002261, Russian Foundation for Basic Research;
                Award ID: 14-04-00638
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002261, Russian Foundation for Basic Research;
                Award ID: 15-34-20490
                Award Recipient :
                The collection of material and study of musculature was supported by the Russian Foundation for Basic Research (project nos. 14-04-00638, 15-34-20490); the rest of the study was supported by the Russian Science Foundation (project no. 14-14-00208).
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Ganglia
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Ganglia
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Anatomy
                Nervous System
                Central Nervous System
                Medicine and Health Sciences
                Anatomy
                Nervous System
                Central Nervous System
                Biology and Life Sciences
                Anatomy
                Nervous System
                Medicine and Health Sciences
                Anatomy
                Nervous System
                Biology and Life Sciences
                Zoology
                Animal Anatomy
                Wings
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Physiology
                Biology and Life Sciences
                Zoology
                Animal Physiology
                Invertebrate Physiology
                Insect Physiology
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Cranium
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Cranium
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Abdominal Muscles
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Abdominal Muscles
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                All relevant data are within the paper and its Supporting Information files.

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