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Wing shape variations in an invasive moth are related to sexual dimorphism and altitude

Published online by Cambridge University Press:  27 January 2010

N. Hernández-L.
Affiliation:
PUCE, Facultad de Ciencias Exactas y Naturales, Quito, Ecuador
Á.R. Barragán
Affiliation:
PUCE, Facultad de Ciencias Exactas y Naturales, Quito, Ecuador
S. Dupas
Affiliation:
PUCE, Facultad de Ciencias Exactas y Naturales, Quito, Ecuador IRD-UR 072, Biodiversité et évolution des complexes plantes – insectes ravageurs – antagonistes, LEGS, UPR 9034, CNRS 91198Gif-sur Yvette Cedex, France and Université Paris-Sud 11, 91405Orsay Cedex, France
J.-F. Silvain
Affiliation:
IRD-UR 072, Biodiversité et évolution des complexes plantes – insectes ravageurs – antagonistes, LEGS, UPR 9034, CNRS 91198Gif-sur Yvette Cedex, France and Université Paris-Sud 11, 91405Orsay Cedex, France
O. Dangles*
Affiliation:
PUCE, Facultad de Ciencias Exactas y Naturales, Quito, Ecuador IRD-UR 072, Biodiversité et évolution des complexes plantes – insectes ravageurs – antagonistes, LEGS, UPR 9034, CNRS 91198Gif-sur Yvette Cedex, France and Université Paris-Sud 11, 91405Orsay Cedex, France
*
*Author for correspondence Fax: (593) 2991687 E-mail: dangles@legs.cnrs-gif.fr

Abstract

Wing morphology has great importance in a wide variety of aspects of an insect's life. Here, we use a geometric morphometric approach to test the hypothesis that variation, in insect wing morphology patterns, occurs between sexes and along altitudinal gradients for invasive species, despite their recent association to this environment. We explored the variation in wing morphology between 12 invasive populations of the invasive potato pest, Tecia solanivora, at low and high altitude in the central highlands of Ecuador. After characterizing sexual dimorphism in wing shape, we investigated if moths at higher elevations differ in wing morphology from populations at lower altitudes. Results indicate wing shape and size differences between sexes and between altitudinal ranges. Females showed larger, wider wings than males, while high altitude moths showed larger, narrow-shaped wings by comparison to low-altitude moths. GLM analyses confirmed altitude was the only significant determinant of this gradient. Our study confirms a sexual dimorphism in size and wing shape for the potato moth. It also confirms and extends predictions of morphological changes with altitude to an invasive species, suggesting that wing morphology variation is an adapted response contributing to invasion success of the potato moth in mountainous landscapes. Ours is one of the first studies on the morphology of invasive insects and represents a valuable contribution to the study of insect invasions because it both offers empirical support to previous genetic studies on T. solanivora as well as proving broader insight into the mechanisms behind morphological evolution of a recently introduced pest.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2010

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References

Adams, D.C., Rohlf, F.J. & Slice, D.E. (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 46, 180194.Google Scholar
Altshuler, D.L. & Dudley, R. (2002) The ecological evolutionary interface of hummingbird flight physiology. Journal of Experimental Biology 205, 23252336.CrossRefGoogle ScholarPubMed
Arnqvist, G. & Martensson, T. (1998) Measurement error in geometric morphometrics: empirical strategies to assess and reduce its impact on measure of shape. Acta Zoologica Academiae Scientarum Hungaricae 44, 7396.Google Scholar
Barragán, A. (2005) Identificación, Biología y Comportamiento de las Polillas de la papa en el Ecuador. 12 pp. Quito, Ecuador, Boletín PROMSA, MAG-PUCE.Google Scholar
Baylac, M., Villemant, C. & Simbolotti, G. (2003) Combining geometric morphometrics with pattern recognition for the investigation of species complexes. Biological Journal of the Linnean Society 80, 8998.CrossRefGoogle Scholar
Berwaerts, K., Van Dyck, H. & Aerts, P. (2002) Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Functional Ecology 16, 484491.CrossRefGoogle Scholar
Berwaerts, K., Aerts, P. & Van Dyck, H. (2006) On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria. Biological Journal of the Linnean Society 89, 675687.CrossRefGoogle Scholar
Betts, C.R. & Wootton, R.J. (1988) Wing shape and flight behaviour in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): a preliminary analysis. Journal of Experimental Biology 138, 271288.CrossRefGoogle Scholar
Blanckenhorn, W.U. & Demont, M. (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integrative and Comparative Biology 44, 413424.CrossRefGoogle ScholarPubMed
Bookstein, F.L. (1991) Morphometric Tools for Landmark Ddata: Geometry and Biology. 435 pp. New York: Cambridge University Press.Google Scholar
Borror, D.J., De Long, D.M. & Triplehorn, C.A. (1981) Introduction to the Study of Insects. 5th edn.827 pp. Philadelphia, PA, USA, CBS College Publishing.Google Scholar
Breuker, C.J., Brakefield, P.M. & Gibbs, M. (2007) The association between wing morphology and dispersal is sex-specific in the glanville fritillary butterfly Melitaea cinxia (Lepidoptera: Nymphalidae). European Journal of Entomology 104, 445452.CrossRefGoogle Scholar
Cáceres, L., Mejía, R. & Ontaneda, G. (1998) Evidencias del cambio climático en Ecuador. Bulletin Français des Etudes Andines 27, 547556.CrossRefGoogle Scholar
Calvo, D. & Molina, J. (2005) Fecundity-body size relationship and other reproductive aspects of Streblote panda (Lepidoptera: Lasiocampidae). Annals of the Entomological Society of America 98, 191196.CrossRefGoogle Scholar
Cardini, A. & O'Higgins, P. (2004) Patterns of morphological evolution in Marmota (Rodentia, Sciuridae): geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation. Biological Journal of the Linnean Society 82, 385407.CrossRefGoogle Scholar
Carreira, V.P., Soto, I.M., Hasson, E. & Fanara, J.J. (2006) Patterns of variation in wing morphology in the cactophiilic Drosophila buzzatii and its sibling D. kowpferae. Journal of Evolutionary Biology 19, 12751282.CrossRefGoogle Scholar
Cavalcanti, M.J., Monteiro, L.R. & Duarte-L., P.R. (1999) Landmark-based morphometric analysis in selected species of Serranid fishes (Perciformes: Teleostei). Zoological Studies 38, 287294.Google Scholar
Dangles, O., Carpio, C., Barragan, A.R., Zeddam, J.L. & Silvain, J.F. (2008) Temperature as a key driver of ecological sorting among invasive pest species in the tropical Andes. Ecological Applications 18, 17951809.CrossRefGoogle ScholarPubMed
Dillon, M.E. & Frazier, M.R. (2006) Drosophila melanogaster locomotion in cold thin air. Journal of Experimental Biology 209, 364371.CrossRefGoogle ScholarPubMed
Douwes, P. (1976) Activity in Heodes virgaureae (Lepidoptera: Lycaenidae) in relation to air temperature, solar radiation, and time of day. Oecologia 22, 287298.CrossRefGoogle Scholar
EPPO/OEPP (2005) Data sheet on quarantine pests: Tecia solanivora. EPPO/OEPP Bulletin 35, 399401.CrossRefGoogle Scholar
Frazier, M.R., Harrison, J.F., Kirkton, S.D. & Roberts, S.P. (2008) Cold rearing improves cold-flight performance in Drosophila via changes in wing morphology. Journal of Experimental Biology 221, 21162122.CrossRefGoogle Scholar
Gilchrist, G.W. (1990) The consequences of sexual dimorphism in body size for butterfly flight and thermoregulation. Functional Ecology 4, 475487.CrossRefGoogle Scholar
Gilchrist, G.W. & Huey, R.B. (2004) Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila suboscura. Integrative and Comparative Biology 44, 461470.CrossRefGoogle Scholar
Gomez, J.L.JR. & Monteiro, L.R. (2008) Morphological divergence patterns among populations of Poecilia vivipara: test of an ecomorphological paradigm. Biological Journal of the Linnean Society 93, 799812.CrossRefGoogle Scholar
Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica 4, 9 pp.Google Scholar
Hodkinson, I.D. (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biology Reviews 80, 489513.CrossRefGoogle ScholarPubMed
Hoffmann, A.A., Collins, E. & Woods, R.E. (2002) Wing shape and wing size changes as indicators of environmental stress in Helicoverpa punctigera (Lepidoptera: Noctuidae) moths: comparing shifts in means, variances and asymmetries. Environmental Entomology 31, 965971.CrossRefGoogle Scholar
Hoffmann, A.A., Woods, R.E., Collins, E., Wallin, K., White, A. & McKenzie, J.A. (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Australian Journal of Entomology 44, 233243.CrossRefGoogle Scholar
Hughes, C.L., Dytham, C. & Hill, J.K. (2007) Modelling and analyzing evolution of dispersal in populations at expanding range boundaries. Ecological Entomology 32, 437445.CrossRefGoogle Scholar
Kingsolver, J.G. (1983) Ecological significance of flight activity in Colias butterflies: implications of reproductive strategy and population structure. Ecology 64, 546551.CrossRefGoogle Scholar
Klimov, P.B., Bochkov, A.V. & O'Connor, B.M. (2006) Host specificity and multivariate diagnostic of cryptic species in predacious cheyletid mites of the genus Cheletophyes (Acari: Cheyletidae) associated with large carpenter bees. Biological Journal of the Linnean Society 87, 4558.CrossRefGoogle Scholar
Loh, R., David, J.R., Debat, V. & Bitner-Mathé, B.C. (2008) Adaptation to different climates results in divergent phenotypic plasticity of wing size and shape in an invasive drosophilid. Journal of Genetics 87, 209217.CrossRefGoogle Scholar
Miller, E.E. (1991a) Positive relation between body size and altitude of capture site in tortricid moths (Tortricidae). Journal of the Lepidopterists' Society 45, 6667.Google Scholar
Miller, E.E. (1991b) Body size in North American Lepidoptera as related to geography. Journal of the Lepidopterists' Society 45, 158168.Google Scholar
Moraes, E.M., Manfrin, M.H., Laus, A.C., Rosada, R.S., Bomfin, S.C. & Sene, F.M. (2004) Wing shape heritability and morphological divergence of the sibling species Drosophila mercatorum and Drosophila paranaensis. Heredity 92, 466473.CrossRefGoogle ScholarPubMed
Muralimohan, K. & Srinivasa, Y.B. (2008) Occurrence of protandry in an aseasonal multivoltine moth: Implications for body-size evolution. Current Science 94, 513518.Google Scholar
Niño, L. (2004) Revisión sobre la polilla de la papa Tecia solanivora en Centro y Sudamérica. Suplemento Revista Latinoamericana de la papa, 4–22.Google Scholar
Norry, F.M., Bubliy, O.A. & Loeschchke, V. (2001) Developmental time, body size and wing loading in Drosophila buzzatii from lowland and highland populations in Argentina. Hereditas 135, 3540.CrossRefGoogle ScholarPubMed
Notz, A. (1996) Influencia de la temperatura sobre la biología de Tecia solanivora Povolny (Lepidoptera: Gelechiidae) criadas en tubérculos de papa Solanum tuberosum L. Boletín Entomología Venezolana 11, 4954.Google Scholar
Nylin, S. & Gotthard, K. (1998) Plasticity in life-history traits. Annual Review of Entomology 43, 6383.CrossRefGoogle ScholarPubMed
Nylin, S., Wiklund, C., Wickman, P.O. & Garcia-Barros, E. (1993) Absence of tradeoffs between sexual size dimorphism and early male emergence in a butterfly. Ecology 74, 14141427.CrossRefGoogle Scholar
Pollet, A., Barragán, A., Zeddam, J.-L. & Lery, X. (2003) Tecia solanivora, a serious biological invasion of potato cultures in South America. International Pest Control 45, 139144.Google Scholar
Povolny, D. (1973) Scrobipalpopsis solanivora sp. n. –A new pest of potato (Solanum tuberosum) from Central America. Acta Universitatis Agriculturae, Facultas Agronomica 21, 143146.Google Scholar
Pruna, A.M. (2004) Comportamiento y control de polillas de la papa (Tecia solanivora, Symmetrischema tangolias y Phthorimaea operculella) en el valle de Salcedo. PhD thesis, Technical University of Cotopaxi, Latacunga, Ecuador.Google Scholar
Puillandre, N., Dupas, S., Dangles, O., Zeddam, J.-L., Capdevielle-Dulac, C., Barbin, K., Torres-Leguizamon, M. & Silvain, J.F. (2007) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biological Invasions 10, 319333.CrossRefGoogle Scholar
Pumisacho, M. & Sherwood, S. (2002) El Cultivo de la papa en Ecuador. 229 pp. Quito, Ecuador, INIAP and CIP.Google Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. Vienna, Austria, Foundation for Statistical Computing.Google Scholar
Rohlf, F.J. (1990) Morphometrics. Annual Review of Ecology and Systematics 21, 299316.CrossRefGoogle Scholar
Rohlf, F.J. (1993) Relative warp analysis and an example to its application to mosquito wings. pp. 131159in Marcus, L.F., Bello, E. & García-Valdecasas, A. (Eds) Contributions to Morphometrics. Madrid, Spain, Museo Nacional de Ciencias Naturales, CSIC.Google Scholar
Rohlf, F.J. (1999) Shape statistics: Procrustes superimposition and tangent spaces. Journal of Classification 16, 197223.CrossRefGoogle Scholar
Rohlf, F.J. (2003) TpsSmall. Version 1.20. New York, Department of Ecology and Evolution, State University of New York. Available at http://morph.bio.sunysb.edu/morph/index.html (accessed 2 July 2008).Google Scholar
Rohlf, F.J. (2004) TpsSpline. Thin-plate spline, Version 1.20. New York, Department of Ecology and Evolution, State University of New York. Available at http://morph.bio.sunysb.edu/morph/index.html (accessed 2 July 2008).Google Scholar
Rohlf, F.J. (2005) TpsRegr. Version 1.31. New York, Department of Ecology and Evolution, State University of New York. Available at http://morph.bio.sunysb.edu/morph/index.html (accessed 2 July 2008).Google Scholar
Rohlf, F.J. (2006) TpsDig. Version 2.10. New York, Department of Ecology and Evolution, State University of New York. Available at http://morph.bio.sunysb.edu/morph/index.html (accessed 2 July 2008).Google Scholar
Rohlf, F.J. (2007) TpsRelw. Version 1.45. New York, Department of Ecology and Evolution, State University of New York. Available at http://morph.bio.sunysb.edu/morph/index.html (accessed 2 July 2008).Google Scholar
Rohlf, F.J. & Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology and Evolution 8, 129132.CrossRefGoogle Scholar
Rohlf, F.J., Loy, A. & Corti, M. (1996) Morphometric analysis of Old World Talpidae (Mammalia, Insectivora) using partial warp scores. Systematic Biology 45, 344362.CrossRefGoogle Scholar
Shreeve, T.G. (1984) Habitat selection, mate location, and microclimatic constraints on the activity of the speckled wood butterfly, Pararge aegeria. Oikos 42, 371377.CrossRefGoogle Scholar
Singer, M.C. (1982) Sexual selection for small size in male butterflies. American Naturalist 119, 440443.CrossRefGoogle Scholar
Soto, I.M., Hasson, E.R. & Manfrin, M.H. (2008) Wing morphology is related to host plants in cactophilic Drosophila gouveai and Drosophila antonietae (Diptera, Drosophilidae). Biological Journal of the Linnean Society 95, 655665.CrossRefGoogle Scholar
Stjernholm, F., Karlsson, B. & Boggs, C.L. (2005) Age-related changes in thoracic mass: possible reallocation of resources to reproduction in butterflies. Biological Journal of the Linnean Society 86, 363380.CrossRefGoogle Scholar
Taylor, P.D. & Merriam, G. (1995) Wing morphology of a forest damselfly is related to landscape structure. Oikos 73, 4348.CrossRefGoogle Scholar
Venables, W.N. & Ripley, B.D. (2002) Modern Applied Statistics with S. 4th edn.495 pp. New York, Springer.CrossRefGoogle Scholar
Walker, J.A. (2000) Ability of geometric morphometric methods to estimate a known covariance matrix. Systematic Biology 49, 686696.CrossRefGoogle ScholarPubMed
Willmott, A.P. & Ellington, C.P. (1997) The mechanics of flight in the hawkmoth Manduca sexta. II. Aerodynamic consequences of kinematic and morphological variation. Journal of Experimental Biology 200, 27232745.CrossRefGoogle ScholarPubMed
Wootton, R.J. (1992) Functional morphology of insect wings. Annual Review of Entomology 37, 113140.CrossRefGoogle Scholar
Zelditch, M.L., Swiderski, D.L., Sheets, H.D. & Fink, W.L. (2004) Geometric Morphometrics for Biologists: A Primer. 443 pp. New York, Elsevier Academic Press.Google Scholar