ALLOMETRIC SHAPE CHANGES INDICATE SIGNIFICANT DIVERGENCE IN THE WING SHAPE BETWEEN ASEXUAL AND SEXUAL LINEAGES OF LYSIPHLEBUS FABARUM (MARSHALL) (HYMENOPTERA: BRACONIDAE)
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Dec 30, 2014
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Abstract
We used landmark-based geometric morphometrics to explore and quantify the forewing shape variation between asexual and sexual lineages of Lysiphlebus fabarum aphid parasitoids. We found a significant divergence in wing size and wing shape between the two reproductive lineages. Static allometry, which denotes size-related shape changes measured in different individuals at the same developmental stage within a population or species, accounts for the significant amount of variation in wing shape within each lineage (11.16 % in asexual, 7.5% in sexual). The allometric shape changes appear to be lineage specific, i.e., the allometric slopes of wing shape significantly diverge between lineages. Such a pattern indicates that asexual and sexual lineages differ in the covariation pattern of the wing shape. Further studies on larger datasets, including other Lysiphlebus taxa and closely related groups, would shed more light on the pattern of morphological variation and the significance of the reproductive mode on the morphological evolution of parasitoid wasps.
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Žikić, V., Petrović, A., & Ivanović, A. (2014). ALLOMETRIC SHAPE CHANGES INDICATE SIGNIFICANT DIVERGENCE IN THE WING SHAPE BETWEEN ASEXUAL AND SEXUAL LINEAGES OF LYSIPHLEBUS FABARUM (MARSHALL) (HYMENOPTERA: BRACONIDAE). Acta Entomologica Serbica, 19(1/2), 53-62. Retrieved from https://aes.bio.bg.ac.rs/index.php/aes/article/view/21
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References
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BELSHAW, R., QUICKE, D.L.J., VOLKL, W. & GODFRAY, H.C.J., 1999. Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution, 53: 1189-1199.
DEROCLES, S.A.P., LE RALEC, A., PLANTEGENEST, M., CHAUBET, B., CRUAUD, C., CRUAUD, A. & RASPLUS, J.Y., 2012. Identification of molecular markers for DNA barcoding in the Aphidiinae (Hymenoptera: Braconidae). Molecular Ecology Resources, 12: 197-208.
DOLPHIN, K. & QUICKE, D.L.J., 2001. Estimating the global species richness of an incompletely described taxon: An example using parasitoid wasps (Hymenoptera: Braconidae). Biological Journal of the Linnean Society, 73: 279-286.
DRAKE, A.G. & KLINGENBERG, C.P., 2008. The pace of morphological change: Historical transformation of skull shape in St. Bernard dogs. Proceedings of the Royal Society, B: Biological Sciences, 275: 71–76.
DRYDEN, I.L. & MARDIA, K.V., 1998. Statistical Shape Analysis. Wiley, New York, 376 pp.
GOULD, S.J., 1966. Allometry and size in ontogeny and phylogeny. Biological Reviews, 41: 587-640.
KALDEH, R.S., HOSSEINI, R., HAJIZADEH, J & SOHANI, M.M., 2012. Molecular identification and detection of Lysiphlebus fabarum (Hymenoptera: Braconidae): a key parasitoid of aphids, by using polymerase chain reaction. Journal of Agricultural Sciences and Technology, 14: 1453-1463.
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KLINGENBERG, C.P., 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11: 353-357.
KLINGENBERG, C.P., 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix, 24: 15-24.
MITROVSKI-BOGDANOVIĆ, A., IVANOVIĆ, A., TOMANOVIĆ, Ž., ŽIKIĆ, V., STARÝ, P. & KAVALLIERATOS, N.G., 2009. Sexual dimorphism in Ephedrus persicae (Hymenoptera: Braconidae: Aphidiinae): intraspecific variation in size and shape. Canadian Entomologist, 141: 550-560
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RAKHSHANI, E, STARÝ, P. & TOMANOVIĆ, Ž., 2013. Tritrophic associations and taxonomic notes on Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae), a keystone aphid parasitoid in Iran. Archives of Biological Sciences, Belgrade, 65(2): 667-680.
ROHLF, F.J., 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution, 55: 2143-2160.
ROHLF, F.J., 2005. TpsDig program, version 2.04, Ecology and Evolution, SUNY at Stony Brook. State University of New York, New York.
[Available through: http://life.bio.sunysb.edu/morph/]
ROHLF, F.J. & SLICE, D.E., 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39: 40-59.
SANDROCK, C. & VORBURGER, C., 2011. Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Current Biology, 21(5): 433-437.
SANDROCK, C., FRAUENFELDER, N., VON BURG, S. & VORBURGER, C., 2007. Microsatellite DNA markers for the aphid parasitoid Lysiphlebus fabarum and their applicability to related species. Molecular Ecology Resources, 7(6): 1080–1083.
SANDROCK, C., SCHIRRMEISTER, B. & VORBURGER, C., 2011. Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC Evolutionary Biology, 11: 348.
SCHMID, M., SIEBER, R., ZIMMERMANN, Y.-S. & VORBURGER, C., 2012. Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology, 26: 207-215.
STARÝ, P., 1986. Specificity of parasitoids (Aphidiidae) to the black bean aphid, Aphis fabae complex, in agroecosystems. Acta Entomologica Bohemoslovaca, 83(1): 24–29.
STARÝ, P., 1988. Aphidiidae. in: Minks A.K., Harewijn P. (ed.) World Crop Pests. Aphids. Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, B: 171-184.
STARÝ, P., 1999. Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae). Journal of Applied Entomology, 123(4): 231-235.
STARÝ, P., 2006. Aphid Parasitiods of the Czech Republic. Academia, Prague.
STARÝ, P., RAKHSHANI, E., TOMANOVIĆ, Ž. & HIEMPEL, G.E., 2010. New species of Lysiphlebus Förster 1862 (Hymenoptera: Braconidae: Aphidiinae) attacking soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) from China. Journal of Hymenoptera Research, 19(1): 184-191.
TOMANOVIĆ Ž., KOS, K., PETROVIĆ, A., STARÝ, P., KAVALLIERATOS, N.G., ŽIKIĆ, V., JAKŠE, J. TRDAN, S. & IVANOVIĆ, A. 2013. The relationship between molecular variation and variation in the wing shape of three aphid parasitoid species: Aphidius uzbekistanicus Luzhetzki, Aphidius rhopalosiphi De Stefani Perez and Aphidius avenaphis (Fitch) (Hymenoptera: Braconidae: Aphidiinae). Zoologischer Anzeiger, 252(1): 41-47.
WEI, Y., YU-QIANG, X., XUE-JUN, L., BIAO, X., YAN-ZHOU, Z. & XIN-MING, Y., 2011. Laboratory observations on biological characteristics of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae), a parasitoid of Aphis glycines Matsumura (Hemiptera: Aphididae). Acta Entomologica Sinica, 54(10): 1204-1210.
YU, D.S., VAN ACHTERBERG, C. & HORSTMANN, K., 2012. World Ichneumonoidea 2011. Taxonomy, biology, Morphology and distribution (Braconidae). Taxapad (Scientific names for information management) Interactive catalogue on DVD/CDROM. Vancouver.
ŽIKIĆ, V., TOMANOVIĆ, Ž., KAVALLIERATOS, N.G., STARÝ, P. & IVANOVIĆ, A., 2010. Does allometry account for shape variability in Ephedrus persicae Froggatt (Hymenoptera: Braconidae: Aphidiinae) parasitic wasps? Organisms Diversity and Evolution, 10: 373–380.
ŽIKIĆ, V., TOMANOVIĆ, Ž., IVANOVIĆ, A., KAVALLIERATOS, N.G., STARÝ, P., STANISAVLJEVIĆ, LJ. & RAKHSHANI, E., 2009. Morphological characterization of Ephedrus persicae biotypes (Hymenoptera, Braconidae, Aphidiinae) in the Palaearctic. Annals of the Entomological Society of America, 102(1): 1-11.
BARAHOEI, H., MADJDZADEH, S.M. & MEHRPARVAR, M., 2011. Morphometric differentiation of five biotypes of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae) in Iran. Zootaxa, 2745: 43-52.
BELSHAW, R., QUICKE, D.L.J., VOLKL, W. & GODFRAY, H.C.J., 1999. Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution, 53: 1189-1199.
DEROCLES, S.A.P., LE RALEC, A., PLANTEGENEST, M., CHAUBET, B., CRUAUD, C., CRUAUD, A. & RASPLUS, J.Y., 2012. Identification of molecular markers for DNA barcoding in the Aphidiinae (Hymenoptera: Braconidae). Molecular Ecology Resources, 12: 197-208.
DOLPHIN, K. & QUICKE, D.L.J., 2001. Estimating the global species richness of an incompletely described taxon: An example using parasitoid wasps (Hymenoptera: Braconidae). Biological Journal of the Linnean Society, 73: 279-286.
DRAKE, A.G. & KLINGENBERG, C.P., 2008. The pace of morphological change: Historical transformation of skull shape in St. Bernard dogs. Proceedings of the Royal Society, B: Biological Sciences, 275: 71–76.
DRYDEN, I.L. & MARDIA, K.V., 1998. Statistical Shape Analysis. Wiley, New York, 376 pp.
GOULD, S.J., 1966. Allometry and size in ontogeny and phylogeny. Biological Reviews, 41: 587-640.
KALDEH, R.S., HOSSEINI, R., HAJIZADEH, J & SOHANI, M.M., 2012. Molecular identification and detection of Lysiphlebus fabarum (Hymenoptera: Braconidae): a key parasitoid of aphids, by using polymerase chain reaction. Journal of Agricultural Sciences and Technology, 14: 1453-1463.
KAVALLIERATOS, N.G., LYKOURESSIS, D.P., SARLIS, G.P., STATHAS, G.J., SANCHIS-SEGOVIA, A. & ATHANASSIOU, C.G., 2001. The Aphidiinae (Hymenoptera: Ichneumonoidea: Braconidae) of Greece. Phytoparasitica, 29: 306-340.
KAVALLIERATOS, N.G., TOMANOVIĆ, Ž., STARÝ, P., ATHANASSIOU, C.G., SARLIS, G.P., PETROVIĆ, O., NIKETIĆ, M. & VERONIKI, M.A., 2004. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology, 39: 527–563.
KLINGENBERG, C.P., 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11: 353-357.
KLINGENBERG, C.P., 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix, 24: 15-24.
MITROVSKI-BOGDANOVIĆ, A., IVANOVIĆ, A., TOMANOVIĆ, Ž., ŽIKIĆ, V., STARÝ, P. & KAVALLIERATOS, N.G., 2009. Sexual dimorphism in Ephedrus persicae (Hymenoptera: Braconidae: Aphidiinae): intraspecific variation in size and shape. Canadian Entomologist, 141: 550-560
MITROVSKI-BOGDANOVIĆ, A., PETROVIĆ, A., MITROVIĆ, M., IVANOVIĆ, A., ŽIKIĆ, V., STARÝ, P., VORBURGER, C. & TOMANOVIĆ, Ž., 2013. Identification of two cryptic species within the Praon abjectum group (Hymenoptera: Braconidae: Aphidiinae) using molecular markers and geometric morphometrics. Annals of the Entomological Society of America, 106(2): 170-180.
RAKHSHANI, E, STARÝ, P. & TOMANOVIĆ, Ž., 2013. Tritrophic associations and taxonomic notes on Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae), a keystone aphid parasitoid in Iran. Archives of Biological Sciences, Belgrade, 65(2): 667-680.
ROHLF, F.J., 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution, 55: 2143-2160.
ROHLF, F.J., 2005. TpsDig program, version 2.04, Ecology and Evolution, SUNY at Stony Brook. State University of New York, New York.
[Available through: http://life.bio.sunysb.edu/morph/]
ROHLF, F.J. & SLICE, D.E., 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39: 40-59.
SANDROCK, C. & VORBURGER, C., 2011. Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Current Biology, 21(5): 433-437.
SANDROCK, C., FRAUENFELDER, N., VON BURG, S. & VORBURGER, C., 2007. Microsatellite DNA markers for the aphid parasitoid Lysiphlebus fabarum and their applicability to related species. Molecular Ecology Resources, 7(6): 1080–1083.
SANDROCK, C., SCHIRRMEISTER, B. & VORBURGER, C., 2011. Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC Evolutionary Biology, 11: 348.
SCHMID, M., SIEBER, R., ZIMMERMANN, Y.-S. & VORBURGER, C., 2012. Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology, 26: 207-215.
STARÝ, P., 1986. Specificity of parasitoids (Aphidiidae) to the black bean aphid, Aphis fabae complex, in agroecosystems. Acta Entomologica Bohemoslovaca, 83(1): 24–29.
STARÝ, P., 1988. Aphidiidae. in: Minks A.K., Harewijn P. (ed.) World Crop Pests. Aphids. Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, B: 171-184.
STARÝ, P., 1999. Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae). Journal of Applied Entomology, 123(4): 231-235.
STARÝ, P., 2006. Aphid Parasitiods of the Czech Republic. Academia, Prague.
STARÝ, P., RAKHSHANI, E., TOMANOVIĆ, Ž. & HIEMPEL, G.E., 2010. New species of Lysiphlebus Förster 1862 (Hymenoptera: Braconidae: Aphidiinae) attacking soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) from China. Journal of Hymenoptera Research, 19(1): 184-191.
TOMANOVIĆ Ž., KOS, K., PETROVIĆ, A., STARÝ, P., KAVALLIERATOS, N.G., ŽIKIĆ, V., JAKŠE, J. TRDAN, S. & IVANOVIĆ, A. 2013. The relationship between molecular variation and variation in the wing shape of three aphid parasitoid species: Aphidius uzbekistanicus Luzhetzki, Aphidius rhopalosiphi De Stefani Perez and Aphidius avenaphis (Fitch) (Hymenoptera: Braconidae: Aphidiinae). Zoologischer Anzeiger, 252(1): 41-47.
WEI, Y., YU-QIANG, X., XUE-JUN, L., BIAO, X., YAN-ZHOU, Z. & XIN-MING, Y., 2011. Laboratory observations on biological characteristics of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae), a parasitoid of Aphis glycines Matsumura (Hemiptera: Aphididae). Acta Entomologica Sinica, 54(10): 1204-1210.
YU, D.S., VAN ACHTERBERG, C. & HORSTMANN, K., 2012. World Ichneumonoidea 2011. Taxonomy, biology, Morphology and distribution (Braconidae). Taxapad (Scientific names for information management) Interactive catalogue on DVD/CDROM. Vancouver.
ŽIKIĆ, V., TOMANOVIĆ, Ž., KAVALLIERATOS, N.G., STARÝ, P. & IVANOVIĆ, A., 2010. Does allometry account for shape variability in Ephedrus persicae Froggatt (Hymenoptera: Braconidae: Aphidiinae) parasitic wasps? Organisms Diversity and Evolution, 10: 373–380.
ŽIKIĆ, V., TOMANOVIĆ, Ž., IVANOVIĆ, A., KAVALLIERATOS, N.G., STARÝ, P., STANISAVLJEVIĆ, LJ. & RAKHSHANI, E., 2009. Morphological characterization of Ephedrus persicae biotypes (Hymenoptera, Braconidae, Aphidiinae) in the Palaearctic. Annals of the Entomological Society of America, 102(1): 1-11.