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Insect Morphology in the Age of Phylogenomics: Innovative Techniques and Its Future Role in Systematics

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Insect Morphology in the Age of Phylogenomics: Innovative Techniques and Its Future Role in Systematics bs_bs_banner Entomological Science (2014) 17, 1–24 doi:10.1111/ens.12053 REVIEW ARTICLE Insect morphology in the age of phylogenomics: innovative techniques and its future role in systematics Frank FRIEDRICH1, Yoko MATSUMURA2, Hans POHL2, Ming BAI2,3, Thomas HÖRNSCHEMEYER4 and Rolf G. BEUTEL2 1Biozentrum Grindel und Zoologisches Museum, Universität Hamburg, Hamburg, Germany, 2Entomology Group, Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Jena, Germany, 3Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; and 4Institut für Zoologie und Anthropologie der Universität Göttingen, Göttingen, Germany Abstract A brief account of the history of insect morphology is given. Different techniques and analytical methods used in current projects on insect morphology and phylogeny and their optimized combined application are described. These include fixation, dissection, maceration, histology (microtome sectioning), scanning electron microscopy (SEM), transmission electron microscopy (TEM), serial block-face scanning electron microscopy (SBFSEM), focused ion beam scanning electron microscopy (FIB/SEM), confocal laser scanning microscopy (CLSM), bleaching, micro-computed tomography (μCT), computer-based three-dimensional reconstruction, focus stacking of digital images, geometric morphometrics and the storage of morphological metadata. The role of insect morphology in the “age of phylogenomics” is discussed. Key words: confocal laser scanning microscopy, dissection, electron microscopy, focus stacking of digital images, geometric morphometrics, histology, micro computed tomography. INTRODUCTION (1994), but without mentioning that “Morphologie” was coined by the German poet Johann Wolfgang von After a marked decline in the last decades of the last Goethe in 1779, and later independently by the German century, research in insect morphology and anatomy has anatomist Karl Friedrich Burdach in 1800. In contrast enjoyed a remarkable renaissance in the last ten years. to anatomy (Greek: aná = on, tomé = cut; investigation Innovative methods and new theoretical concepts have of the shape structure, and position of organs or body given new strong impulses to this discipline. An over- parts) morphology (Greek: morphé = form, shape, view of more traditional and modern techniques and lógos = word, teaching, ratio) always implies a com- their optimal combination is the main topic of this parative aspect and the concept of homology plays an contribution. important role. A detailed account of the history of insect mor- We owe the earliest scientific entomological infor- phology and anatomy was presented by Gupta (1994). mation to the famous Greek philosopher and natura- Therefore the historical development will be outlined list Aristotle (384–322 BCE). Among other groups of only briefly here. The different meanings of the terms animals, insects are also treated in his eminent work De morphology and anatomy were pointed out by Gupta Partibus Animalicum. However, the outstanding scholar pointed out that insects were so insignificant that they weren’t worth of the types of investigations dedicated Correspondence: Yoko Matsumura, Entomology Group, to vertebrates such as “fish”, “reptiles” and mammals. Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, In Western Europe the roots of scientific entomology Erbertstr.1, 07743 Jena, Germany. and insect morphology go back to the 17th century. Email: [email protected] In 1669 the Dutch naturalist, anatomist and micro- Received 20 June 2013; accepted 28 July 2013. scopist Jan Swammerdam (1637–1680) published his © 2013 The Entomological Society of Japan F. Friedrich et al. remarkable book Historia Insectorum Generalis (“The (Weber 1933) and Grundriss der Insektenkunde (Weber Natural History of Insects”), focused on the develop- 1938) ). A highly productive but controversial North ment and metamorphosis of insects. Swammerdam’s American entomologist of the early 20th century was investigations were remarkably modern, already charac- Guy Chester Crampton (e.g. Crampton 1918, 1928). terized by careful dissections, a comparative approach Very important morphological contributions were made and the efficient use of microscopy. A prominent by another American insect morphologist, Gordon Italian researcher of this century was Marcello Malpighi Floyd Ferris. The understanding of thoracic structures (1628–1694) who discovered the excretory tubules was greatly improved by his profound studies (e.g. Ferris named after him, the insect heart and the anastomosing 1940). tracheal system (Gupta 1994). A distinguished natura- Outstanding morphological studies were published by list and entomologist of the 18th century was August Weber and his students at the University of Tübingen Johann Rösel von Rosenhof who published numerous (e.g. Wenk 1953; Weber 1955, 1960). The exceptional beautiful illustrations of insects and other arthropods beauty and detail-richness of the illustrations in Weber’s including developmental stages and, in some cases, also posthumously published monograph on the elephant anatomical details. His famous Insecten-Belustigung louse (Weber 1969) are still unsurpassed, and a similar (“Insect Amusement”) was published in 1740. He degree of perfection was reached by other members of already attempted to use a natural classification and can his group (e.g. Bierbrodt 1942). The tradition of the be considered as one of the founders of entomology in Weber school was continued by Gerhard Mickoleit (e.g. Germany. Many of Carl von Linné’s later descriptions of Mickoleit 1961, 1963) and students under his supervi- insects are based on Rösel’s work. Eminent entomolo- sion (e.g. Burmeister 1976; Rieger 1976). Another out- gists of the 18th century were Johann Christian Fabri- standing school of insect morphologists was the group cius and Pierre Latreille. However, their focus was more of Jean Chaudonneret at the Department d’Entmologie on classification than on morphology in a stricter sense. of the University of Dijon, France. Brilliant contri- An outstanding insect anatomist of the 18th century was butions were published by Chaudonneret himself Pierre Lyonnet (1708–1789) who described the incred- (e.g. Chaudonneret 1948, 1950–51) but also by some ible number of 1647 muscles in the goat moth (Cossus of his co-workers (e.g. Bitsch 1966). A fascinating and cossus) and discovered the peritrophic membrane, ima- extremely detailed anatomical study on the alder fly ginal discs and the prothoracic glands in the caterpillar Chauliodes formosanus was carried out by Takadi Maki (Tuxen 1973; Gupta 1994). at the former Imperial Taihoku University (Maki 1936). Carl Hermann Conrad Burmeister (1807–1892) was Another remarkable contribution by a Japanese insect an exceptional entomologist, zoologist and paleontolo- morphologist was the three-volume work on the evolu- gist of the 18th century. He published the first volume tion of the insect head, thorax and abdomen by Ryuichi of the Handbuch der Entomologie (Burmeister 1832), Matsuda (Matsuda 1965, 1970, 1976). The work was a remarkable contribution that was later translated mainly based on the results of earlier morphological into English (Gupta 1994). Charles Janet (1849–1932) studies but extremely useful as a reference work. was not only a dedicated entomologist and owner of The classical tradition of insect morphology was approximately 40 000 fossils, but was also an engineer, upheld at a very high level by scientists at the Zoologisk inventor and company director. Aside from his studies Museum in Copenhagen, notably by the eminent insect on plant biology and evolution he excelled as a pioneer systematist Niels Peder Kristensen. He published not of insect histology. His remarkable treatment of the only outstanding morphological treatments of lepi- anatomy of social insects was mainly based on serial dopteran key taxa (e.g. Kristensen 1968, 1984) and sections of stunning quality (Billen & Wilson 2008). an entire series of profound reviews of insect phylo- Two outstanding entomological works with simple geny (e.g. Kristensen 1975, 1991), but also landmark and virtually identical titles were published in the first volumes on systematics and morphology of Lepidoptera decade of the 20th century, Les Insectes by Louis Félix in the Handbook of Zoology series (Kristensen 1997, Henneguy (1904) and Gli Insetti by Antonio Berlese 2003). (1909). Other milestones in the study of insect structures Morphology-based insect systematics arguably were books published in the 1920s and 1930s by the reached a peak with the publication of the ground- American entomologists Augustus Daniel Imms (A breaking works of the German dipterist Willy Hennig General textbook of Entomology (Imms 1925) ) and (e.g. Hennig 1969), who also revolutionized phyloge- Robert Evans Snodgrass (The Principles of Insect Mor- netic reconstruction (Hennig 1950). In the last decades phology (Snodgrass 1935) ), and by the German mor- of the century, the detailed study of morphological phologist Herrmann Weber (Lehrbuch der Entomologie features of insects, especially internal structures, 2 Entomological Science (2014) 17, 1–24 © 2013 The Entomological Society of Japan Innovative techniques for morphology became less and less popular. This development was TRADITIONAL AND MODERN probably partly correlated with the rise of molecular
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