Geometric morphometrics in entomology: Basics and applications

The recent expansion of a variety of morphometric tools has brought about a revolution in the comparison of morphology in the context of the size and shape in various fields including entomology. First, an overview of the theoretical issues of geometric morphometrics is presented with a caution about the usage of traditional morphometric measurements. Second, focus is then placed on two broad approaches as tools for geometric morphometrics; that is, the landmark‐based and the outline‐based approaches. A brief outline of the two methodologies is provided with some important cautions. The increasing trend of entomological studies in using the procedures of geometric morphometrics is then summarized. Finally, information is provided on useful toolkits such as computer software as well as codes and packages of the R statistical software that could be used in geometric morphometrics.

[1]  R. C. Firman,et al.  Postmating Female Control: 20 Years of Cryptic Female Choice , 2017, Trends in ecology & evolution.

[2]  Takao K Suzuki.  Modularity of a leaf moth-wing pattern and a versatile characteristic of the wing-pattern ground plan , 2013, BMC Evolutionary Biology.

[3]  F. Rohlf,et al.  Morphometric Spaces, Shape Components and the Effects of Linear Transformations , 1996 .

[4]  W. Atchley,et al.  Ratios and the Statistical Analysis of Biological Data , 1978 .

[5]  L. F. Marcus,et al.  Advances in Morphometrics , 1996, NATO ASI Series.

[6]  D L Brower,et al.  Engrailed gene expression in Drosophila imaginal discs. , 1986, The EMBO journal.

[7]  A. Shapiro,et al.  THE LOCK-AND-KEY HYPOTHESIS: EVOLUTIONARY AND BIOSYSTEMATIC INTERPRETATION OF INSECT GENITALIA , 1989 .

[8]  D. Martín-Vega,et al.  Looking into the puparium: Micro‐CT visualization of the internal morphological changes during metamorphosis of the blow fly, Calliphora vicina, with the first quantitative analysis of organ development in cyclorrhaphous dipterans , 2017, Journal of morphology.

[9]  Erik Otárola-Castillo,et al.  geomorph: an r package for the collection and analysis of geometric morphometric shape data , 2013 .

[10]  G. P. Lohmann.  Eigenshape analysis of microfossils: A general morphometric procedure for describing changes in shape , 1983 .

[11]  F. Rohlf,et al.  A revolution morphometrics. , 1993, Trends in ecology & evolution.

[12]  F. James Rohlf,et al.  The tps series of software , 2015 .

[13]  Fernanda Bribiesca-Contreras,et al.  Three-dimensional visualisation of the internal anatomy of the sparrowhawk (Accipiter nisus) forelimb using contrast-enhanced micro-computed tomography , 2017, PeerJ.

[14]  Anuj Srivastava,et al.  Statistical Shape Analysis , 2014, Computer Vision, A Reference Guide.

[15]  J. Mosimann,et al.  NEW STATISTICAL METHODS FOR ALLOMETRY WITH APPLICATION TO FLORIDA RED‐WINGED BLACKBIRDS , 1979, Evolution; international journal of organic evolution.

[16]  V. Debat,et al.  Wing morphology of the active flyer Calliphora vicina (Diptera: Calliphoridae) during its invasion of a sub-Antarctic archipelago where insect flightlessness is the rule , 2016 .

[17]  R. Beutel,et al.  A review of methods for analysing insect structures - the role of morphology in the age of phylogenomics. , 2016, Current opinion in insect science.

[18]  D. Ahrens,et al.  Asymmetry in genitalia does not increase the rate of their evolution. , 2015, Molecular phylogenetics and evolution.

[19]  Pete E. Lestrel,et al.  Fourier Descriptors and their Applications in Biology , 2008 .

[20]  Daniel Martín-Vega,et al.  The ‘dance’ of life: visualizing metamorphosis during pupation in the blow fly Calliphora vicina by X-ray video imaging and micro-computed tomography , 2017, Royal Society Open Science.

[21]  C. Klingenberg.  MorphoJ: an integrated software package for geometric morphometrics , 2011, Molecular ecology resources.

[22]  G. Struhl,et al.  Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. , 1995, Development.

[23]  H. Krapp,et al.  A quantitative comparison of micro-CT preparations in Dipteran flies , 2016, Scientific Reports.

[24]  R. Ray,et al.  Enhanced flight performance by genetic manipulation of wing shape in Drosophila , 2016, Nature Communications.

[25]  T. P. Burnaby.  Growth-Invariant Discriminant Functions and Generalized Distances , 1966 .

[26]  H. Niemeyer,et al.  X‐ray computed tomography reveals that intraspecific competition promotes soldier differentiation in a one‐piece nesting termite , 2017 .

[27]  Paul Galpern,et al.  Automated measurement of Drosophila wings , 2003, BMC Evolutionary Biology.

[28]  A. Austin,et al.  Novel use of a micro‐computed tomography scanner to trace larvae of wood boring insects , 2011 .

[29]  R. Beutel,et al.  Comparative thoracic anatomy of the wild type and wingless (wg1cn1) mutant of Drosophila melanogaster (Diptera). , 2016, Arthropod structure & development.

[30]  Cédric Gaucherel,et al.  Momocs: Outline Analysis Using R , 2014 .

[31]  Y. Okada,et al.  DEFICIENCY MAPPING OF THE GENOMIC REGIONS ASSOCIATED WITH EFFECTS ON DEVELOPMENTAL STABILITY IN DROSOPHILA MELANOGASTER , 2011, Evolution; international journal of organic evolution.

[32]  King-Sun Fu,et al.  Shape Discrimination Using Fourier Descriptors , 1977, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[33]  J. Rasplus,et al.  When morphometry meets genetics: inferring the phylogeography of Carabus solieri using Fourier analyses of pronotum and male genitalia , 2004, Journal of evolutionary biology.

[34]  Pete E Lestrel,et al.  Morphometrics for the life sciences , 2000 .

[35]  F. Bookstein,et al.  Morphometric Tools for Landmark Data: Geometry and Biology , 1999 .

[36]  F. Bookstein.  Combining the Tools of Geometric Morphometrics , 1996 .

[37]  A. Hidalgo.  Three distinct roles for the engrailed gene in Drosophila wing development , 1994, Current Biology.

[38]  C. Klingenberg.  Size, shape, and form: concepts of allometry in geometric morphometrics , 2016, Development Genes and Evolution.

[39]  Root anatomy and canal morphology of mandibular first premolars in a Chinese population , 2017, Scientific Reports.

[40]  F. Rohlf.  Geometric morphometrics simplified , 2005 .

[41]  Karen Lu.  HARMONIC ANALYSIS OF THE HUMAN FACE. , 1965, Biometrics.

[42]  Charles R. Giardina,et al.  Elliptic Fourier features of a closed contour , 1982, Comput. Graph. Image Process..

[43]  A. Garcı́a-Bellido,et al.  Developmental analysis of the wing disc in the mutant engrailed of Drosophila melanogaster. , 1972, Genetics.

[44]  S. Ferson,et al.  Measuring shape variation of two-dimensional outlines , 1985 .

[45]  V. Fernandez,et al.  Aspects of gorgonopsian paleobiology and evolution: insights from the basicranium, occiput, osseous labyrinth, vasculature, and neuroanatomy , 2017, PeerJ.

[46]  S. Cohen,et al.  Early development of leg and wing primordia in the Drosophila embryo , 1991, Mechanisms of Development.

[47]  Christian Peter Klingenberg,et al.  Evolution and development of shape: integrating quantitative approaches , 2010, Nature Reviews Genetics.

[48]  S. Lele.  Euclidean Distance Matrix Analysis (EDMA): Estimation of mean form and mean form difference , 1993 .

[49]  Philip J. Withers,et al.  Metamorphosis revealed: time-lapse three-dimensional imaging inside a living chrysalis , 2013, Journal of The Royal Society Interface.

[50]  D'arcy W. Thompson,et al.  On Growth and Form , 1917, Nature.

[51]  J. Gurdon,et al.  Morphogen gradient interpretation , 2001, Nature.

[52]  S. Vadlamani.  On the Diffusion of Shape , 2007 .

[53]  C. Goodall.  Procrustes methods in the statistical analysis of shape , 1991 .

[54]  A. Córdoba‐Aguilar,et al.  Sexual selection and animal genitalia. , 2004, Trends in ecology & evolution.

[55]  J. P. Masly,et al.  170 Years of “Lock-and-Key”: Genital Morphology and Reproductive Isolation , 2011, International journal of evolutionary biology.

[56]  Farah Ahmed,et al.  Exploring miniature insect brains using micro-CT scanning techniques , 2016, Scientific Reports.

[57]  Evangelos E. Milios,et al.  Optimal spline fitting to planar shape , 1994, Signal Process..

[58]  W. Eberhard,et al.  SPECIES ISOLATION, GENITAL MECHANICS, AND THE EVOLUTION OF SPECIES‐SPECIFIC GENITALIA IN THREE SPECIES OF MACRODACTYLUS BEETLES (COLEOPTERA, SCARABEIDAE, MELOLONTHINAE) , 1992, Evolution; international journal of organic evolution.

[59]  Takeshi Hayashi,et al.  Genomic Prediction of Biological Shape: Elliptic Fourier Analysis and Kernel Partial Least Squares (PLS) Regression Applied to Grain Shape Prediction in Rice (Oryza sativa L.) , 2015, PloS one.

[60]  P. Lawrence,et al.  Compartments in the wing of Drosophila: a study of the engrailed gene. , 1976, Developmental biology.

[61]  P. Goloboff,et al.  Phylogenetic morphometrics (I): the use of landmark data in a phylogenetic framework , 2010, Cladistics : the international journal of the Willi Hennig Society.

[62]  G. Uhl,et al.  A spider mating plug: origin and constraints of production , 2014 .

[63]  Fred L. Bookstein,et al.  MULTIVARIATE DISCRIMINATION BY SHAPE IN RELATION TO SIZE , 1981 .

[64]  D. Bolnick,et al.  Predictable Patterns of Disruptive Selection in Stickleback in Postglacial Lakes , 2008, The American Naturalist.

[65]  P. Brennan,et al.  Sperm storage: distinguishing selective processes and evaluating criteria. , 2015, Trends in ecology & evolution.

[66]  H. Iwata,et al.  SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. , 2002, The Journal of heredity.

[67]  T. Daniel,et al.  The Journal of Experimental Biology 206, 2979-2987 © 2003 The Company of Biologists Ltd , 2022 .

[68]  R. Beutel,et al.  Insect morphology in the age of phylogenomics: innovative techniques and its future role in systematics , 2014 .

[69]  F. Rohlf,et al.  A COMPARISON OF FOURIER METHODS FOR THE DESCRIPTION OF WING SHAPE IN MOSQUITOES (DIPTERA: CULICIDAE) , 1984 .

[70]  Peter N. Schweitzer,et al.  Parametric cubic splines and geologic shape descriptions , 1985 .

[71]  David G. Kendall,et al.  Shape & Shape Theory , 1999 .

[72]  Alexander C. Dobens,et al.  FijiWings: An Open Source Toolkit for Semiautomated Morphometric Analysis of Insect Wings , 2013, G3: Genes, Genomes, Genetics.

[73]  D. Berner.  Size correction in biology: how reliable are approaches based on (common) principal component analysis? , 2011, Oecologia.

[74]  M. Wolfner,et al.  Correction for Mattei et al., Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning , 2017, Proceedings of the National Academy of Sciences.

[75]  S. Shapiro,et al.  An Analysis of Variance Test for Normality (Complete Samples) , 1965 .

[76]  H. Tatsuta,et al.  Relationship between size and shape in the sexually dimorphic beetle Prosopocoilus inclinatus (Coleoptera: Lucanidae) , 2004 .

[77]  Morphometric Studies on the Variation of Male Lucanid Beetle Mandibles , 2013 .

[78]  T. Tabata,et al.  Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs , 1994, Cell.

[79]  J. Sekelsky,et al.  Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed. , 1995, Genetics.

[80]  L. Penrose.  Distance, size and shape. , 1954, Annals of eugenics.

[81]  Peter J. Gregory,et al.  Tracking larval insect movement within soil using high resolution X‐ray microtomography , 2004 .

[82]  H. David Sheets,et al.  Geometric morphometrics for biologists : a primer , 2004 .

[83]  Horst Engels.  A least squares method for estimation of Bezier curves and surfaces and its applicability to multivariate analysis , 1986 .

[84]  Qingbin Zhan,et al.  A tool for developing an automatic insect identification system based on wing outlines , 2015, Scientific Reports.

[85]  W. Atchley,et al.  Statistical Properties of Ratios. I. Empirical Results , 1976 .

[86]  A. Siegel,et al.  A robust comparison of biological shapes. , 1982, Biometrics.

[87]  Luis M. Escudero,et al.  Imaginal discs , 2010, Current Biology.

[88]  Pablo A. Goloboff,et al.  TNT, a free program for phylogenetic analysis , 2008 .

[89]  Franklin A. Graybill,et al.  Introduction to the Theory of Statistics, 3rd ed. , 1974 .

[90]  Lísa Anne Libungan,et al.  ShapeR: An R Package to Study Otolith Shape Variation among Fish Populations , 2015, PloS one.

[91]  Christian Peter Klingenberg,et al.  Morphological Integration and Developmental Modularity , 2008 .

[92]  Z B Zeng,et al.  Genetic architecture of a morphological shape difference between two Drosophila species. , 2000, Genetics.

[93]  Greg Gibson,et al.  Epidermal Growth Factor Receptor and Transforming Growth Factor-β Signaling Contributes to Variation for Wing Shape in Drosophila melanogaster , 2006, Genetics.

[94]  C. R. Deboor,et al.  A practical guide to splines , 1978 .

[95]  Imran A. Rahman,et al.  Experimental reduction of intromittent organ length reduces male reproductive success in a bug , 2015, Proceedings of the Royal Society B: Biological Sciences.

[96]  W. Potthast,et al.  Musculoskeletal modelling of the dragonfly mandible system as an aid to understanding the role of single muscles in an evolutionary context , 2016, Journal of Experimental Biology.

[97]  G. Gibson,et al.  Association Between Nucleotide Variation in Egfr and Wing Shape in Drosophila melanogaster , 2004, Genetics.

[98]  Xianzhong Feng,et al.  Evolution through genetically controlled allometry space. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[99]  L. Knowles,et al.  Correlated evolution of multivariate traits: detecting co‐divergence across multiple dimensions , 2007, Journal of evolutionary biology.

[100]  A. R. Ennos.  THE IMPORTANCE OF TORSION IN THE DESIGN OF INSECT WINGS , 1988 .

[101]  C. Botto-Mahan,et al.  POLLINATOR-MEDIATED SELECTION ON THE NECTAR GUIDE PHENOTYPE IN THE ANDEAN MONKEY FLOWER, MIMULUS LUTEUS , 2003 .

[102]  D. Kendall.  SHAPE MANIFOLDS, PROCRUSTEAN METRICS, AND COMPLEX PROJECTIVE SPACES , 1984 .

[103]  A. Hoffmann,et al.  Environmental Stress-Dependent Effects of Deletions Encompassing Hsp70Ba on Canalization and Quantitative Trait Asymmetry in Drosophila melanogaster , 2011, PloS one.

[104]  R. Wootton.  FUNCTIONAL MORPHOLOGY OF INSECT WINGS , 1992 .

[105]  S. J. Arnold,et al.  THE MEASUREMENT OF SELECTION ON CORRELATED CHARACTERS , 1983, Evolution; international journal of organic evolution.

[106]  Julien Claude,et al.  Morphometrics with R , 2009 .

[107]  J. Engler,et al.  Contrasting genetic and morphologic responses on recent population decline in two burnet moths (Lepidoptera, Zygaenidae) , 2012, Conservation Genetics.

[108]  Ralph Roskies,et al.  Fourier Descriptors for Plane Closed Curves , 1972, IEEE Transactions on Computers.

[109]  Andone Estonba,et al.  Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch , 2011, Apidologie.

[110]  Fred L. Bookstein,et al.  A Comment on Shearing as a Method for “Size Correction” , 1987 .

[111]  T. K. Carne,et al.  Shape and Shape Theory , 1999 .

[112]  A. Loy.  Morphometrics and Theriology. Homage to Marco Corti , 2008 .

[113]  Norman MacLeod,et al.  Generalizing and extending the eigenshape method of shape space visualization and analysis , 1999, Paleobiology.