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Wing Shape Variation in the Taxonomic Recognition of Species of Diachlorus Osten-Sacken (Diptera: Tabanidae) from Colombia

  • Systematics, Morphology and Physiology
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Abstract

We evaluated the directional asymmetry between right and left wings and quantified the intraspecific and interspecific variation of the wing shape of 601 specimens of the genus Diachlorus to determine to what extent the geometrical variation discriminates six species distributed in six protected areas of Colombia. Geometric analyses were performed, integrating Procrustes methods, principal component analyses, cluster analyses, linear and quadratic discriminant analyses, and evaluations of shape changes. In Diachlorus, left and right wings did not present significant asymmetry but a geometrical analysis was allowed for species identification and, in some cases, the origin of the specimens using the variation of wing shape; the best-assigned species was Diachlorus leticia Wilkerson & Fairchild, while the worst was Diachlorus jobbinsi Fairchild, which also had the highest intraspecific variation, while Diachlorus fuscistigma Lutz had the lowest variation. Diachlorus fuscistigma and Diachlorus leucotibialis Wilkerson & Fairchild were the most similar species, while D. leucotibialis and Diachlorus nuneztovari Fairchild & Ortiz were the most disimilar. The specimens with the most different wing shape belonged to Chocó (especially those of D. jobbinsi), the geographically farthest area from the others in the study; however, no correlation was observed between geometric and geographical distances. Linear discriminants were better than nonlinear (quadratic) discriminant analyses in predicting species membership, but the opposite was true for predicting area membership. Based on our data, we hypothesized that other species of Diachlorus could also be discriminated using geometric morphometry of the wing shape.

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References

  • Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Hystrix 24(1):7–14

    Google Scholar 

  • Adams DC, Otarola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Meth Ecol Evol 4:393–399

    Article  Google Scholar 

  • Bolnick DI, Amarasekare P, Araújo MS, Burger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26(4):183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Bookstein FL (1989) Principal warps: thin-plate splines and the decomposition of deformations. IEEE Trans Pattern Anal Mach Intell 11:567–585

    Article  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York, p 435

    Google Scholar 

  • Buestán J, Navarrete R, Mejia M (2007) Lista actualizada de Tábanos (Diptera: Tabanidae) del Ecuador. Rev Ecuat Hig Med Trop 44(1):23–63

    Google Scholar 

  • Calinsky T, Harabasz J (1974) A dendrite method for cluster analysis. Commun Stat - Theory and Methods 3(1):1–27

    Article  Google Scholar 

  • Campos DF, Fernández F (2002) El proyecto “Diversidad de Insectos en Colombia”. Proyecto de red Iberoamericana de Biogeografía y Entomología Sistemática PrIBES. m3m Monografías Tercer Milenio, España, pp 297–300

    Google Scholar 

  • Cárdenas RE, Buestán J, Dangles O (2009) Diversity and distribution models of horse flies (Diptera: Tabanidae) from Ecuador. Ann Soc Entomol Fr (ns) 45(4):511–528

    Google Scholar 

  • Cárdenas RE, Hérnandez-L N, Barragán A, Dangles O (2013) Differences in morphometry and activity among tabanid fly assemblages in an Andean tropical montane cloud forest: indication of altitudinal migration? Biotropica 45(1):63–72

    Article  Google Scholar 

  • Cardini A, Elton S (2007) Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology 126:121–134

    Article  Google Scholar 

  • Charrad M, Ghazzali N, Boiteau V, Niknafs A (2014) NbClust: an R package for determining the relevant number of cluster in a data set. J Stat Softw 61(6):1–36

    Article  Google Scholar 

  • Coscarón S, Philip CB (1979) A revision of Mycteromyiini (“genus Mycteromyia” of authors), a new tribe of Neotropical horse flies (Diptera, Tabanidae). Proc Calif Acad Sci 41:427–452

    Google Scholar 

  • Coscarón S, Papavero N (1993) An illustrated manual for the identification of the Neotropical genera and subgenera of Tabanidae (Diptera). Museu Paraense Emilio Goeldi, Coleção Emilie Snethlage, Museu Paraense Emílio Goeldi, Belém, p 150

    Google Scholar 

  • Coscarón S, Papavero N (2009a) Manual of Neotropical Diptera. Tabanidae Neotrop Dipter 6:1–137

    Google Scholar 

  • Coscarón S, Papavero N (2009b) Catalogue of Neotropical Diptera. Tabanidae Neotrop Dipter 16:1–199

    Google Scholar 

  • Coscarón S, Papavero N (2014) Key to the known immature stages of Neotropical Tabanidae. Neotrop Dipter 24:1–22

    Google Scholar 

  • De la Riva J, Le Pont F, Ali V, Matias A, Mollinedo S, Dujardin JP (2001) Wing geometry as a tool for studying the Lutzomyia longipalpis (Diptera: Psychodidae) complex. Mem Inst Oswaldo Cruz 96(8):1089–1094

    Article  PubMed  Google Scholar 

  • Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, Chichester, p 376

    Google Scholar 

  • Dryden IL (2013) Shapes: statistical shape analysis. R package version 1.1-9. URL http://CRAN.R-project.org/package=shapes

  • Dujardin JP, Le Pont F, Martinez E (1999) Quantitative morphological evidence for incipient species within Lutzomyia quinquefer (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 94(6):829–836

    Article  CAS  PubMed  Google Scholar 

  • Fairchild GB, Philip CB (1960) A revision of the Neotropical genus Dichelacera subgenus Dichelacera Macquart (Diptera, Tabanidae). Stud Entomol 3(1–4):83

    Google Scholar 

  • Fairchild GB (1969) Notes on Neotropical Tabanidae (Diptera) XII. Classification and distribution, with keys to genera and subgenera. Arq Zool S Paulo 17(4):199–255

    Article  Google Scholar 

  • Fairchild GB (1972) Notes on Neotropical Tabanidae (Diptera) XIII. The genus Diachlorus O.S. Fla. Entomol 55(4):219–229

    Google Scholar 

  • Fisher RA (1936) The use of multiple measurements in taxonomic problems. Ann Eugenics 7:179–188

    Article  Google Scholar 

  • Fraley C, Raftery AE (2002) Model-based clustering, discriminant analysis and density estimation. J Am Stat Assoc 97:611–631

    Article  Google Scholar 

  • Fraley C, Raftery AE (2007) Model-based methods of classification: using the mclust software in chemometrics. J Stat Softw 18(6):1–13

    Article  Google Scholar 

  • Franco FF, Soto IM, Sene FM, Manfrin MH (2008) Phenotypic variation of the aedeagus of Drosophila serido Vilela & Sene (Diptera: Drosophilidae). Neotrop Entomol 37(5):558–563

    Article  PubMed  Google Scholar 

  • González CR (2004) Agelanius verai, a new species of horse fly from Chile (Diptera: Tabanidae). Zootaxa 571:1–5

    Google Scholar 

  • González CR (2006) Description of male and redescription of the female of Veprius fulvus Coscarón, Philip & Fairchild, 1979 (Diptera: Tabanidae: Pangoniini). Acta Entomol Chil 30:39–42

    Google Scholar 

  • González CR (2009) Agelanius chiloensis, a new species of horse fly from southern Chile (Diptera: Tabanidae). Gayana 73:12–16

    Google Scholar 

  • González CR (2014) Two new species of the genus Dasybasis Macquart, 1847, from Chile (Diptera: Tabanidae: Diachlorini). Zootaxa 3893(2):293–300

    Article  PubMed  Google Scholar 

  • Goodall C (1991) Procrustes methods in the statistical analysis of shape. J R Stat Soc Ser B (Methodological) 53:285–339

    Google Scholar 

  • Gorayeb IS, Gómes ZT, Velásquez-de-Rios M (2013) Description of a new species of Stenotabanus from Venezuela (Diptera: Tabanidae). Boletim do Museu Paraense Emílio Goeldi Ciências Naturais 8:41–47

    Google Scholar 

  • Gorayeb IS (2014) Tabanidae (Diptera) of Amazonia XXI. Descriptions of Elephantotus gen. n. and E. tracuateuensis sp. n. (Diachlorini) from the Brazilian coast. ZooKeys 395:23–31

    Article  Google Scholar 

  • Gower JC (1975) Generalized Procrustes analysis. Psychometrika 40:33–51

    Article  Google Scholar 

  • Henriques AL, Rafael JA (1993) Revisão do gênero Neotropical Acanthocera Macquart (Diptera: Tabanidae). Acta Amazon 23(4):403–440

    Article  Google Scholar 

  • Henriques AL, Rafael JA (1999) Tabanidae (Diptera) from Parque Nacional do Jaú, Amazonas, Brazil, with description of two new species of Diachlorus Osten Sacken. In: Burger EJF (ed) Memoirs on entomology international: contributions to the knowledge of Diptera: a collection of articles on Diptera commemorating the life and work of Graham B. Fairchild. Associated, Florida, pp 195–222

    Google Scholar 

  • Henriques AL (2006) O gênero Philipotabanus Fairchild (Insecta: Diptera: Tabanidae) na Amazônia, com chave para as fêmeas das espécies e descrição de P. obidensis sp. nov. Acta Amazon 36(4):549–556

    Article  Google Scholar 

  • Henriques AL, Krolow TK, Rafael JA (2012) Corrections and additions to catalogue of Neotropical Diptera (Tabanidae) of Coscarón & Papavero (2009). Rev Bras Entomol 56(3):277–280

    Article  Google Scholar 

  • Henriques AL, Krolow TK (2013) Description of Muscotabanus gen. nov. and M. rafaeli sp. nov. (Diptera: Tabanidae: Diachlorini) from Amazon Basin, Brazil. Mem Inst Oswaldo Cruz 108:383–385

    Article  PubMed Central  Google Scholar 

  • Ihaka R, Murrell P, Hornik K, Fisher J, Zeileis A (2013) Colorspace: color space manipulation. R package version 1.2-4. URL http://CRAN.R-project.org/package=colorspace

  • Jablonski D (2000) Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology. Paleobiology (suppl) 26:15–52

    Article  Google Scholar 

  • Jaramillo ON, Dujardin JP, Calle-Londoño D, Fonseca-González I (2014) Geometric morphometrics for the taxonomy of 11 species of Anopheles (Nyssorhynchus) mosquitoes. Med Vet Entomol 29:26–36

    Article  Google Scholar 

  • Kendall DG (1984) Shape manifolds, procrustean metrics and complex projective spaces. Bull Lond Math Soc 16:81–121

    Article  Google Scholar 

  • Klingenberg CP, McIntyre GS, Zaklan SD (1998) Left-right asymmetry of fly wings and the evolution of body axes. Proc R Soc Lond B 265:1255–1259

    Article  CAS  Google Scholar 

  • Krolow TK, Henriques AL (2009) Descrição de uma nova espécie de Chlorotabanus (Insecta, Diptera, Tabanidae) da Região Neotropical. Iheringia. Série Zoologia 99:204–209

    Article  Google Scholar 

  • Krolow TK, Henriques AL (2010) Taxonomic revision of the New World genus Chlorotabanus Lutz, 1913 (Diptera: Tabanidae). Zootaxa 2656:1–40

    Google Scholar 

  • Krolow TK, Henriques AL, Gorayeb IS, Limeira-de-Oliveira F, Buestán J (2015) Taxonomic revision of the Neotropical genus Pityocera Giglio-Tos, 1896 (Diptera: Tabanidae: Scionini). Zootaxa 3904:1–301

    Article  Google Scholar 

  • Lane RP, Marshall J (1981) Geographical variation, races and subspecies. In: Forey PL (ed) The evolving biosphere. British Museum (Natural History), London, pp 9–19

    Google Scholar 

  • Lessard BD, Cameron SL, Bayless KM, Wiegmann BM, Yeates DK (2013) The evolution and biogeography of the austral horse fly tribe Scionini (Diptera: Tabanidae: Pangoniinae) inferred from multiple mitochondrial and nuclear genes. Mol Phylo Evol 68(3):516–540

    Article  CAS  Google Scholar 

  • Limeira-de-Oliveira F, Henriques AL, Gorayeb IS (2009) Tabanidae (Diptera) do estado do Maranhão, Brasil IV. Descrição de Dichelacera (Dichelacera) gemmae sp.n.1. Neotrop Entomol 38:104–107

    Article  Google Scholar 

  • Lorenz C, Suesdek L (2013) Short report: evaluation of chemical preparation on insect wing shape for geometric morphometrics. Am J Trop Med Hyg 89(5):928–931

    Article  PubMed  PubMed Central  Google Scholar 

  • Mackerras IM (1954) The classification and distribution of Tabanidae (Diptera). I. General review. Aust J Zool 2:431–454

    Article  Google Scholar 

  • Mackerras IM (1955) The classification and distribution of Tabanidae (Diptera). II. History, morphology, classification. Subfamily Pangoniinae. Aust J Zool 3:439–511

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2):209–220

    CAS  PubMed  Google Scholar 

  • McLachlan GJ, Peel D (2000) Finite mixture models. Wiley series in probability and statistics. New York, p 419

  • McQuitty LL (1966) Similarity analysis by reciprocal pairs for discrete and continuous data. Educ Psychol Meas 26:825–831

    Article  Google Scholar 

  • Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K (2014) Cluster: cluster analysis basics and extensions. R package version 1.15.2. URL http://CRAN.R-project.org/package=cluster

  • Morita SI (2008) A phylogeny of long-tongued horse flies (Diptera: Tabanidae: Philoliche) with the first cladistic review of higher relationships within the family. Invertebr Syst 22:311–327

    Article  Google Scholar 

  • Murdoch D, Chow ED (2013) Ellipse: functions for drawing ellipses and ellipse-like confidence regions. R package version 0.3-8. URL http://CRAN.R-project.org/package=ellipse

  • Oksanen J, Guillaume-Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10. URL http://CRAN.R-project.org/package=vegan

  • Oney B, Reineking B, O’Neill G, Kreyling J (2013) Intraspecific variation buffers projected climate change impacts on Pinus contorta. Ecol Evol 3(2):437–449

    Article  PubMed  PubMed Central  Google Scholar 

  • Polly PD (2005) Development and phenotypic correlations: the evolution of tooth shape in Sorex araneus. Evol Dev 7:29–41

    Article  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Version 3.1.2. URL http://www.r-project.org/

  • Rafael JA, Marques DWA, Limeira-de-Oliveira F (2012) Tabanidae (Diptera) of Maranhão state, Brazil. V. Description of Protosilvius gurupi sp. n. (Pangoniinae, Pangoniini) and key to Protosilvius species. ZooKeys 235:41–50

    Article  PubMed  Google Scholar 

  • Rohlf FJ (1990) Morphometrics. Annu Rev Ecol Evol Syst 21:299–316

    Article  Google Scholar 

  • Rohlf FJ, Slice DE (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59

    Article  Google Scholar 

  • Rohlf FJ, Marcus LF (1993) A revolution in morphometrics. Trends Ecol Evol 8(4):129–132

    Article  Google Scholar 

  • Rohlf FJ, Bookstein FL (2003) Computing the uniform component of shape variation. Syst Biol 51(1):66–69

    Article  Google Scholar 

  • Roskov Y, Kunze T, Orrell T, Abucay L, Paglinawan L, Culham A, Bailly N, Kirk P, Bourgoin T, Baillargeon G, Decock W, De Wever A, Didžiulis V (eds) (2014) Species 2000 & ITIS catalogue of life, 2014 annual checklist. Digital resource at www.catalogueoflife.org/annual-checklist/2014/. Accessed 25 Jan 2015

  • Roth V, Steinhage V (1999) Nonlinear discriminant analysis using Kernel functions. In: Solla S, Leen T, Müller K (eds) Advances in neural information processing systems. MIT, Cambridge, pp 568–574

    Google Scholar 

  • Runyon JB, Hurley RL (2004) A new genus of long-legged flies displaying remarkable wing directional asymmetry. Proc R Soc Lond B (Suppl) 271:S114–S116

    Article  Google Scholar 

  • Sanchez G (2013) DiscriMiner: tools of the trade fir discriminant analysis. R package version 0.1-29. URL http://CRAN.R-project.org/package=DiscriMiner

  • Savriama Y, Klingenberg CP (2006) Geometric morphometrics of complex symmetric structures: shape analysis of symmetry and asymmetry with Procrustes methods. In: Barber S, Baxter PD, Mardia KV, Walls RE (eds) Interdisciplinary statistics and bioinformatics. Leeds University Press, Leeds, pp 158–161

    Google Scholar 

  • Savriama Y, Klingenberg CP (2011) Beyond bilateral symmetry: geometric morphometric methods for any type of symmetry. BMC Evol Biol 11:280

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheets HD, Covino KM, Panasiewicz JM, Morris SR (2006) Comparison of geometric morphometric outline methods in the discrimination of age-related differences in feather shape. Front Zool 3:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Simons AM (2002) The continuity of microevolution and macroevolution. J Evol Biol 15:688–701

    Article  Google Scholar 

  • Slice DE (2007) Geometric morphometrics. Ann Rev Anthropol 36:261–281

    Article  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. W. H. Freeman and Co., San Francisco, p 573

    Google Scholar 

  • Sokal RR, Sneath PHA (1963) Principles of numerical taxonomy. W. H. Freeman and Co., San Francisco, p 359

    Google Scholar 

  • Solé RV, Manrubia SC, Benton M, Kauffman S, Bak P (1999) Criticality and scaling in evolutionary ecology. Trends Ecol Evol 14:156–160

    Article  PubMed  Google Scholar 

  • Soto IM, Carreira VP, Fanara JJ, Hasson E (2007) Evolution of male genitalia: environment and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids. BMC Evol Biol 7:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Swaddle JP (1997) Within-individual changes in developmental stability affect flight performance. Behav Ecol 8(6):601–604

    Article  Google Scholar 

  • Tibshirani R, Walther G, Hastie T (2001) Estimating the number of clusters in a data set via the gap statistic. J R Stat Soc B 63(2):411–423

    Article  Google Scholar 

  • Tomkins JL, Kotiaho JS (2001) Fluctuating asymmetry. In: Encyclopedia of life sciences. MacMillan Publishers Ltd., Nature Publishing Group, London, pp 1–5

    Google Scholar 

  • Tuffery S (2011) Data mining and statistics for decision making. Wiley, Chichester, p 685

    Book  Google Scholar 

  • Turcatel M, de Carvalho CJB, Rafael JA (2010) A taxonomic revision of Stibasoma Schiner, 1867 (Diptera: Tabanidae). Zootaxa 2368:1–39

    Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S. Fourth edition. Springer, p 498

  • Weaver AA, Schoell SL, Nguyen CM, Lynch SK, Stitzel JD (2014) Morphometric analysis of variation in the sternum with sex and age. J Morphol 275(11):1284–1299

    Article  PubMed  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York, p 213

    Book  Google Scholar 

  • Wiegmann BM, Tsaur SC, Webb DW, Yeates DK, Cassel BK (2000) Monophyly and relationships of the Tabanomorpha (Diptera: Brachycera) based on 28S ribosomal gene sequences. Ann Entomol Soc Am 93(5):1031–1038

    Article  CAS  Google Scholar 

  • Wilkerson RC (1979) Horse flies (Diptera: Tabanidae) of the Colombian departments of Chocó, Valle and Cauca. PhD. Thesis, University of Florida, Florida, p 489

  • Wilkerson RC (1981) Two new species of Dichelacera (Nothocanthocera) Fairchild, with a key to the species of the subgenus (Diptera: Tabanidae). Proc Entomol Soc Wash 83:64–71

    Google Scholar 

  • Wilkerson RC, Fairchild GB (1982) Five new species of Diachlorus (Diptera: Tabanidae) from South America with a revised key to species and new locality records. Proc Entomol Soc Wash 84:636–650

    Google Scholar 

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Acknowledgments

We thank Dr. Augusto Loureiro Henriques and Dr. Tiago Kutter Krolow for helping with specimen identification and Dr. Carlos Eduardo Sarmiento Monroy (ICN-UNAL) and “Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (IavH)” for kindly providing the specimens used in this study. We thank Dr. Santiago Catalano and the two anonymous reviewers for their helpful comments on the manuscript. This research was conducted as a partial requirement for the undergraduate degree of the first author. The second author is indebted to the División de Investigación y Extensión, Facultad de Salud, Universidad Industrial de Santander (project 5658), and the División de Investigación y Extensión, Facultad de Ciencias, Universidad Industrial de Santander (project 5132), for their financial support. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Torres, A., Miranda-Esquivel, D.R. Wing Shape Variation in the Taxonomic Recognition of Species of Diachlorus Osten-Sacken (Diptera: Tabanidae) from Colombia. Neotrop Entomol 45, 180–191 (2016). https://doi.org/10.1007/s13744-015-0350-1

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