Abstract
The present study aimed to determine the wing asymmetry and sexual asymmetry of Pantala flavescens (Fabricius 1798) collected from a paddy field. P. flavescens is known as the longest migratory insect species and the morphological architecture of their hindwing aids in long-distance gliding. In our study, we collected F1 generation of male and female P. flavescens and used for geometric morphometric study to investigate wing asymmetry. We observed no difference in wing size between sexes from the study, but there are significant (p < 0.05) shape differences. The female population was more asymmetric than male population, with a high shape-related fluctuation asymmetry (FA). Discriminant function analysis was used to validate wing asymmetry (right-left) and sexual asymmetry of P. flavescens. Canonical variant analysis discriminated the forewings and hindwings of P. flavescens both sexes in a distinct morphospace. The PC’s warp shape analysis proved that, when compared to forewings, the highest amount of shape variations was observed in hindwings, especially in anal lobe regions. Based on the results, pesticide and fertilizer used in the paddy fields are the primary reason for the high level of FA, and the morphological variations observed in the hindwings may influence the migratory behaviour of P. flavescens.
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All data are included in the main manuscript; additional data are available on reasonable request from the corresponding author.
Change history
06 April 2023
A Correction to this paper has been published: https://doi.org/10.1007/s11756-023-01404-8
References
Abaga NOZ, Alibert P, Dousset S, Savadogo PW, Savadogo M, Sedogo M (2011) Insecticide residues in cotton soils of Burkina Faso and effects of insecticides on fluctuating asymmetry in honey bees (Apis mellifera Linnaeus). Chemosphere 83:585–592. https://doi.org/10.1016/j.chemosphere.2010.12.021
Alibert P, Moureau B, Dommergues J, David B (2001) Differentiation at a microgeographical scale within two species of ground beetle, Carabus auronitens and C. nemoralis (Coleoptera, Carabidae): a geometrical morphometric approach. Zool Scr 30(4):299–311. https://doi.org/10.1046/j.1463-6409.2001.00068.x
Alvial I, Araya J, Araya R, Vila I, Veliz D (2016) Large-scale geographical variation in wings size and wing shape of the cosmopolitan dragonfly Pantala flavescens (Fabricius 1798) (Odonata: Libellulidae). Ph. D thesis. University of Chile, pp 65–86
Anderson RC (2009) Do dragonflies migrate across the western Indian ocean? J Trop Ecol 25:347–358
Barbon MM, Arreza JDZ, Tabugo SRM (2016) Fluctuating asymmetry as an indicator of ecological stress and developmental instability of Neurothemis ramburii ( Odonata : Libellulidae ) in Iligan City, Philippines. J Biol Environ Sci 8(3):142–152
Benitez HA, Lemic D, Puschel TA et al (2018) Fluctuating asymmetry indicates levels of disturbance between agricultural productions: an example in Croatian population of Pterostichus melas melas (Coleptera: Carabidae). Zool Anz 276:42–49. https://doi.org/10.1016/j.jcz.2018.07.003
Benton TG, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687. https://doi.org/10.1046/j.1365-2664.2002.00745.x
Berns CM (2013) The evolution of sexual dimorphism: Understanding mechanisms of sexual shape differences. In: Moriyama H (ed) Sexual Dimorphism. In Tech. https://doi.org/10.5772/55154
Bjorksten T, David P, Pomiankowski A, Fowler K (2000) Fluctuating asymmetry of sexual and nonsexual traits in stalk-eyed flies : a poor indicator of developmental stress and genetic quality. J Evol Biol 13(1):89–97. https://doi.org/10.1046/j.1420-9101.2000.00146.x
Bjorksten TA, Pomiankowski A, Fowler K (2001) Temperature shock during development fails to increase the fluctuating asymmetry of a sexual trait in stalk-eyed flies. Proc R Soc Lond B 268:1503–1510. https://doi.org/10.1098/rspb.2001.1575
Bonada N, Vives S, Rieradevall M, Prat N (2005) Relationship between pollution and fluctuating asymmetry in the pollution-tolerant caddisfly Hydropsyche exocellata (Trichoptera, Insecta). Arch Hydrobiol 162:167–185. https://doi.org/10.1127/0003-9136/2005/0162-0167
Breuker CJ, Gibbs M, Van Dongean S, Merckx T, Van Dyck H (2010) The use of geometric morphometric in studying butterfly wings in an evolutionary ecological context. In: Ashraf MTE (ed) Morphometrics for non morphometricians. Springer-Verlag, Berlin, pp 271–287
Bybee S, Cordoba-Aguilar A, Duryea M, Futahashi R, Hansson B, Lorenzo-Carballa M (2016) Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics. Front Zool 13(46):1–21. https://doi.org/10.1186/s12983-016-0176-7
Cairns J, McCormick PV, Niederlehner BR (1993) A proposed framework for developing indicators of ecosystem health. Hydrobiologica 263:1–44. https://doi.org/10.1007/BF00006084
Carter AJR, Weier TM, Houle D (2009) The effect of inbreeding on fluctuating asymmetry of wing veins in two laboratory strains of Drosophila melanogaster. Heredity 102:563–572. https://doi.org/10.1038/hdy.2009.13
Chang X, Zhai B, Liu X, Wang M (2006) Effects of temperature stress and pesticide exposure on fluctuating asymmetry and mortality of Copera annulata (selys) (Odonata: Zygoptera) larvae. Ecotoxicol Environ Saf 67(1):120–127. https://doi.org/10.1016/j.ecoenv.2006.04.004
Chang X, Zhai B, Wang M, Wang B (2007) Relationship between exposure to an insecticide and fluctuating asymmetry in a damselfly (Odonata, Coenagriidae). Hydrobiologica 586:213–220. https://doi.org/10.1007/s10750-007-0620-y
Chapman JW, Goulson D (2000) Environmental versus genetic influences on fluctuating asymmetry in the housefly, Musca domestica. Biol J Linn Soc Lond 70(3):403–413. https://doi.org/10.1111/j.1095-8312.2000.tb01231.x
Chapman JW, Reynolds DR, Wilson K (2015) Long-range seasonal migration in insects: mechanisms, evolutionary diverse and ecological consequences. Ecol Lett 18(3):287–302. https://doi.org/10.1111/ele.12407
Clarke GM (1993) Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ Pollut 82(2):207–211. https://doi.org/10.1016/0269-7491(93)90119-9
Clarke GM (1995) Relationships between developmental stability and fitness: application for conservation biology. Conserv Biol 9(1):18–24
Clarke GM, Brand CGW, Whittena BMJ (1986) Fluctuating asymmetry : a technique for measuring developmental stress. Aust J Biol Sci 39:145–154
Coda JA, Gomez D, Martinez JJ, Steinmann AR, Priotto J (2016) The use of fluctuating asymmetry as a measure of farming practice effects in rodents: a species-specific response. Ecol Indic 70:269–275. https://doi.org/10.1016/j.ecolind.2016.06.018
Corbert PS (1999) Dragonflies: behaviour and ecology of Odonata. Cornell University Press, New York
Corbet PS (2004) Dragonflies: behaviour and ecology of odonata (revised edition). Harley Books, Colchester
David P, Hingle A, Greig D, Rutherford A, Pomiankowski A, Fowler K (1998) Male sexual ornament size but not asymmetry reflects condition in stalk-eyed flies. Proc R Soc B Lond 265:2211–2216. https://doi.org/10.1098/rspb.1998.0561
Demayo CG, Harun SA, Torres MAJ (2011) Procrustes analysis of wing shape divergence among sibling species of Neurothemic dragonflies. Aust J Basic Appl Sci 5(6):748–759
Fowler K, Whitlock MC (1994) Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity 73:373–376. https://doi.org/10.1038/hdy.1994.184
Fraser FC (1936) The Fauna of British India, including Ceylon and Burma. Odonata. Vols I-III. Taylor and Francis Ltd, London
Fruciano C (2016) Measurement error in geometric morphometrics. Dev Genes Evol 226:139–158. https://doi.org/10.1007/s00427-016-0537-4
Gallesi M, Mobili S, Cigognini R, Hardersen S, Sacchi R (2016) Season matters: differential variation of wing shape between sexes of Calopteryx splendens (Odonata: Calopterygidae). Zoomorphology 135:313–322. https://doi.org/10.1007/s00435-016-0309-8
Garrison RW, Ellenrieder N, Louton JA (2006) Dragonfly genera of the New World. Hopkins University Press, Baltimore
Gibbs M, Wklund C, Van Dyck H (2010) Phenotypic plasticity in butterfly morphology in response to weather conditions during development. J Zool 283:162–168. https://doi.org/10.1111/j.1469-7998.2010.00756.x
Graham JH, Roe KE, West TB (1993) Effects of lead and benzene on developmental stability of Drosophila melanogaster. Ecotoxicology 2:185–195. https://doi.org/10.1007/BF00116423
Gumiel M et al (2003) Wing geometry in Triatoma infestans (Klug) and T. melanosome Martinez, Olmedo & Carcavallo (Hemiptera: Reduviidae). Syst Entomol 28(2):173–180. https://doi.org/10.1046/j.1365-3113.2003.00206.x
Hardersen S, Wratten SD (1998) The effects of Carbaryl exposure of the penultimate larval instars of Xathocnemis Zealandica on emergence and fluctuating asymmetry. Ecotoxicology 7:297–304. https://doi.org/10.1023/A:10088600164
Hedlund JSU, Lv H, Lehmann P, Hu G, Anderson RC, Chapman JW (2021) Unraveling the world’s longest non-stop migration: the Indian Ocean crossing of the globe skimmer dragonfly. Front Ecol Evol 9:698128. https://doi.org/10.3389/fevo.2021.698128
Hobson KA, Anderson RC, Soto DX, Wassenaar LI (2012) Isotopic evidence that dragonflies (Panata flavescens) migrating through the Maldives come from the northern Indian subcontinent. PLoS One 7:e52594. https://doi.org/10.1371/journal.pone.0052594
Hoffmann AA, Collins E, Woods R (2002) Wing shape and wing size changes as indicator of environmental stress in Helicoverpa punctigera (Lepidoptera: Noctuidae) moths: comparing shifts in means, variance, and asymmetries. Environ Entomol 31(6):965–971. https://doi.org/10.1603/0046-225X-31.6.965
Huang S-T, Wang H-R, Yang W-Q et al (2020) Phylogeny of Libellulidae (Odonata: Anisoptrera): comparison of molecular and morphology-based phylogenies based on wing morphology and migration. PeerJ 14(8):e8567. https://doi.org/10.7717/peerj.8567
Imasheva AG, Bosenko DV, Bubli OA (1999) Variation in morphological traits of Drosophila melanogaster (fruit fly) under nutritional stress. Heredity 82:187–192. https://doi.org/10.1038/sj.hdy.6884660
Jentzsch A, Köhler G, Schumacher J (2003) Environmental stress and fluctuating asymmetry in the grasshopper Chorthippus parallelus (Acrididae: Gomphocerinae). Zoology 106(2):117–125. https://doi.org/10.1078/0944-2006-00106
Johansson F, Soderquist M, Bokma F (2009) Insect wing shape evolution: independent effects of migratory and mate guarding flight on dragonfly wings. Biol J Linn Soc Lond 97(2):362–372. https://doi.org/10.1111/j.1095-8312.2009.01211.x
Jones JC, Helliwell P, Beekman M, Maleszka R, Oldroyd BP (2005) The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. J Comp Physiol A 191(12):1121–1129. https://doi.org/10.1007/s00359-005-0035-z
Karthika K, Anand PP, Seena S, Shibu Vardhanan Y (2021) Wing phenotypic plasticity, quantitative genetics, modularity, and phylogenetic signal analysis revealed the niche partitioning in two fruit fly species, Bactrocera dorsalis and Zeugodacus cucurbitae. Int J Trop Insect Sci 42:1487–1504. https://doi.org/10.1007/s42690-021-00668-4
Klingenberg CP (2016) Size, shape, and form: concepts of allometry in geometric morphometrics. Dev Genes Evol 226(3):113–137. https://doi.org/10.1007/s00427-016-0539-2
Lee Y-H, Lin C-P (2012) Morphometric and genetic differentiation of two sibling gossamer-wing damselflies, Euphaca formosa and E. yayeyamana, and adaptive trait divergence in subtropical East Asian islands. J Insect Sci 12:53. https://doi.org/10.1673/031.012.5301
Mahima KV, Anand PP, Seena S, Shameema K, Manogem EM, Shibu Vardhanan Y (2021) Caste-specific phenotypic plasticity of Asian weaver ants: revealing the allometric and non-allometric component of female caste system of Oecophylla smaragdina (Hymenoptera: Formicidae) by using geometric morphometrics. Sociobiology 68(2):e5941. https://doi.org/10.13102/sociobiology.v68i2.5941
May ML (2013) A critical overview of progress in studies of migration of dragonflies (Odonata: Anisoptera), with emphasis on North America. J Insect Conserv 17:1–15. https://doi.org/10.1007/s10841-012-9540-x
Messier S, Mitton JB (1996) Heterozygosity at the malate dehydrogenase locus and developmental homeostasis in Apis mellifera. Heredity 76:616–622. https://doi.org/10.1038/hdy.1996.88
Moller AP (1997) Developmental stability and fitness: a review. Am Nat 149(5):916–932. https://doi.org/10.1086/286030
Monteiro IR (1999) Multivariate regression models and geometric morphometrics: the search for casual factors in the analysis of shape. Syst Biol 48(1):192–199. https://doi.org/10.1080/106351599260526
Outomuro D, Johansson F (2011) The effects of latitude, body size, and sexual selection on wing shape in a damselfly. Biol J Linn Soci 102(2):263–274. https://doi.org/10.1111/j.1095-8312.2010.01591.x
Outomuro D, Bokma F, Johansson F (2012) Hindwing shape evolves faster than front wing shape in Calopteryx damselflies. Evol Biol 39:116–125. https://doi.org/10.1007/s11692-011-9145-4
Outomuro D, Adams DC, Johansson F (2013) The evolution of wing shape in ornamented-winged damselflies (Calopterygidae, Odonata). Evol Biol 40:300–309. https://doi.org/10.1007/s11692-012-9214-3
Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:57–72
Palmer AR, Strobeck C (1997) Fluctuating asymmetry and developmental stability : heritability of observable variation vs. heritability of inferred cause. J Evol Biol 10:39–49. https://doi.org/10.1046/j.1420-9101.1997.10010039.x
Palmer AR, Strobeck C (2003) Fluctuating asymmetry analysis revisited. In: Polak M (ed) Developmental instability (DI): causes and consequences. Oxford University Press, Oxford, pp 279–319
Polak M (1993) Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection. Genetica 89:255–266
Rajabi H, Ghoroubi N, Malaki M, Darvizeh A, Gorb SN (2016) Basal complex and basal venation of odonate wings: structural diversity and potential role in the wing deformation. PLoS One 11(8):e0160610. https://doi.org/10.1371/journal.pone.0160610
Ribeiro B, Guedes RNC, Correa AS, Santos CT (2007) Fluctuating asymmetry in insecticide-resistant and insecticide-susceptible strains of the maize weevil, Sitophilus zeamais (Coleoptera : Curculionidae). Arch Environ Contam Toxicol 53(1):77–83. https://doi.org/10.1007/s00244-006-0162-8
Riget FF, Bechshoft TG, Wiig O, Soone C (2008) Fluctuating asymmetric in metric traits; a practical example of calculating asymmetry, measurement error and repeatability. Ann Zool Fenn 45(1):32–38. https://doi.org/10.5735/086.045.0103
Rohlf FJ (2015) The tps series of software. Hystrix It J Mamm 26(1):9–12. https://doi.org/10.4404/hystrix-26.1-11264
Rohlf FJ, Corti M (2000) The use of two-block partial squares to study covariation in shape. Syst Biol 49(4):740–753. https://doi.org/10.1080/106351500750049806
Ross KG, Robertson JL (1990) Developmental stability, heterozygosity, and fitness in two introduced fire ants (Solenopsis invicta and S . richteri) and their hybrid. Heredity 64:93–103. https://doi.org/10.1038/hdy.1990.12
Roy BA, Stanton ML (1999) Asymmetry of wild mustard, Sinapis arvensis (Brassicaceae), in response to severe physiological stresses. J Evol Biol 12:440–449
Russell RW, May ML, Soltesz KL, Fitzpatrick JW (1998) Massive swarm migrations of dragonflies (Odonata) in eastern North America. Am Midl Nat 140(2):325–342
Sadeghi S, Dumont HJ (2014) Variation in the shape of the wings and taxonomy of Eurasian population of the Calopteryx splendens complex (Odonata: Calopterygidae). Eur J Entomol 111(4):575–583. https://doi.org/10.14411/eje.2014.073
Sanchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020
Stewart SS, Vodopich DS (2018) Environmental effects on wing shape and wing size of Argia sedula (Odonata: Coenagrionidae). Int J Odonatology 21:189–203. https://doi.org/10.1080/13887890.2018.1523752
Strong L, James S (1992) Some effects of rearing the yellow dung fly Scatophaga stercoraria in cattle dung containing ivermectin. Entomol Exp Appl 63:39–45. https://doi.org/10.1111/j.1570-7458.1992.tb02417.x
Suarez-Tovar CM, Sarmiento CE (2016) Beyond the wing planform: morphological differentiation between migratory and nonmigratory dragonfly species. J Evol Biol 29(4):690–703. https://doi.org/10.1111/jeb.12830
Suhling F, Sahlen G, Gorb S, Kalkman VJ, Dijkstra K-DB, van Tol J (2015) Order Odonata. In: Thorp J, Rogers DC (eds) Ecology and general biology: thorp and Covich’s freshwater invertebrates. Academic Press, pp 893–932
Tatalovic LI, Andelic B, Jelic M, Kos T, Benitez HA, Jelaska LS (2020) Fluctuating asymmetry as a method of assessing environmental stress in two predatory carabid species within Mediterranean agroecosystems. Symmetry 12(11):1890. https://doi.org/10.3390/sym12111890
Trotta V, Calboli FCF, Garoia F, Grifoni D, Cavicchi S (2005) Fluctuating asymmetry as a measure of ecological stress in Drosophila melanogaster (Diptera : Drosophilidae). Eur J Entomol 102:195–200. https://doi.org/10.14411/eje.2005.031
Véllestad LA, Hindar K, Méller AP (1999) A meta-analysis of fluctuating asymmetry in relation to heterozygosity. Heredity 83:206–218. https://doi.org/10.1046/j.1365-2540.1999.00555.x
Vijendravarma RK, Narasimha S, Kawecki TJ (2011) Adaptation to larval malnutrition does not affect fluctuating asymmetry in Drosophila melanogaster. Biol J Linn Soc Lond 104(1):19–28. https://doi.org/10.1111/j.1095-8312.2011.01697.x
Villemant C, Simbolotti G, Kenis M (2007) Discrimination of Eubazus (Hymenoptera, Braconidae) sibling species using geometric morphometrics analysis of wing venation. Syst Entomol 32(4):625–634. https://doi.org/10.1111/j.1365-3113.2007.00389.x
Westfall MJ, May ML (2006) Damselflies of North America. Scientific publishers, 2nd edition Inc. Gainesville, Florida
Zikic V, Stankovic SS, Petrovic A, Milosevic M, Tomanovic Z, Klingenberg CP, Ivanovic A (2017) Evolutionary relationship of wing venation and wing size and shape in Aphidiinae (Hymenoptera: Braconidae). Org Divers Evol 17:607–617. https://doi.org/10.1007/s13127-017-0338-2
Acknowledgments
We thank the Department of Zoology, the University of Calicut, for providing the infrastructural facility and UGC-SAP (F.3-6/2012 (SAP-II) dated 10.10.2012). The first author is thankful to the UGC-JRF (F.No.16-9(June 2017)/2018(NET/CSIR) & UGC-Ref. No. 519/(CSIR-UGC NET JUNE 2017), Government of India, for the financial assistance.
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Conceptualization, Conceived and designed the experiment: MG, PPA & YSV. Data collection, Digitalization and landmarking of specimen: MG. Analyzation and interpretation of the data: PPA, MG, & YSV. Wrote the main manuscript: MG & PPA. Drawing & photographic plate preparation: YSV. Supervision: YSV. All authors reviewed the manuscript.
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Gayathri, M., Anand, P.P. & Shibu Vardhanan, Y. Wing size, shape, and asymmetry analysis of the wandering glider, Pantala flavescens (Odonata: Libellulidae) revealed that hindwings are more asymmetric than the forewings. Biologia 78, 2749–2762 (2023). https://doi.org/10.1007/s11756-023-01396-5
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DOI: https://doi.org/10.1007/s11756-023-01396-5