Evolutionary Biology

, Volume 40, Issue 2, pp 300–309

The Evolution of Wing Shape in Ornamented-Winged Damselflies (Calopterygidae, Odonata)

Research Article

Abstract

Flight has conferred an extraordinary advantage to some groups of animals. Wing shape is directly related to flight performance and evolves in response to multiple selective pressures. In some species, wings have ornaments such as pigmented patches that are sexually selected. Since organisms with pigmented wings need to display the ornament while flying in an optimal way, we might expect a correlative evolution between the wing ornament and wing shape. We examined males from 36 taxa of calopterygid damselflies that differ in wing pigmentation, which is used in sexual displays. We used geometric morphometrics and phylogenetic comparative approaches to analyse whether wing shape and wing pigmentation show correlated evolution. We found that wing pigmentation is associated with certain wing shapes that probably increase the quality of the signal: wings being broader where the pigmentation is located. Our results also showed correlated evolution between wing pigmentation and wing shape in hind wings, but not in front wings, probably because hind wings are more involved in signalling than front wings. The results imply that the evolution of diversity in wing pigmentations and behavioural sexual displays might be an important driver of speciation due to important pre-copulatory selective pressures.

Keywords

Geometric morphometrics Phylogeny Sexual signaling Wing pigmentation 

Supplementary material

11692_2012_9214_MOESM1_ESM.doc (152 kb)
Supplementary material 1 (DOC 152 kb)

References

  1. Adams, D. C., & Collyer, M. L. (2007). Analysis of character divergence along environmental gradients and other covariates. Evolution, 61, 510–515.PubMedCrossRefGoogle Scholar
  2. Adams, D. C., & Collyer, M. L. (2009). A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution, 63, 1143–1154.PubMedCrossRefGoogle Scholar
  3. Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology, 10, 216.PubMedCrossRefGoogle Scholar
  4. Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.CrossRefGoogle Scholar
  5. Anderson, C. N., & Grether, G. F. (2010). Character displacement in the fighting colours of Hetaerina damselflies. Proceedings of the Royal Society Series B, 277, 3669–3675.CrossRefGoogle Scholar
  6. Andersson, M. (1994). Sexual selection. Princeton: Princeton University Press.Google Scholar
  7. 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, 675–687.CrossRefGoogle Scholar
  8. 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, 271–288.Google Scholar
  9. Blankers, T., Adams, D. C., & Wiens, J. J. (2012). Ecological radiation with limited morphological diversification in salamanders. Journal of Evolutionary Biology, 25, 634–646.PubMedCrossRefGoogle Scholar
  10. Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745.PubMedGoogle Scholar
  11. Bookstein, F. L. (1991). Morphometric tools for landmark data geometry and biology. Cambridge: Cambridge University Press.Google Scholar
  12. 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, 445–452.Google Scholar
  13. Collyer, M. L., & Adams, D. C. (2007). Analysis of two-state multivariate phenotypic change in ecological studies. Ecology, 88, 683–692.PubMedCrossRefGoogle Scholar
  14. Contreras-Garduño, J., Buzatto, B. A., Serrano-Meneses, M. A., Nájera-Cordero, K., & Córdoba-Aguilar, A. (2008). The size of the red wing spot of the American rubyspot as a heightened condition-dependent ornament. Behavioral Ecology, 19, 724–732.CrossRefGoogle Scholar
  15. Contreras-Garduño, J., Canales-Lazcano, J., & Córdoba-Aguilar, A. (2006). Wing pigmentation, immune ability, fat reserves and territorial status in males of the rubyspot damselfly, Hetaerina americana. Journal of Ethology, 24, 165–173.CrossRefGoogle Scholar
  16. Cordero Rivera, A., Andrés, J. A., Córdoba-Aguilar, A., & Utzeri, C. (2004). Postmating sexual selection: allopatric evolution of sperm competition mechanisms and genital morphology in calopterygid damselflies (Insecta: Odonata). Evolution, 58, 349–359.PubMedGoogle Scholar
  17. Córdoba-Aguilar, A. (2002). Wing pigmentation in territorial male damselflies, Calopteryx haemorrhoidalis: A possible relation to sexual selection. Animal Behaviour, 63, 759–766.CrossRefGoogle Scholar
  18. Córdoba-Aguilar, A., & Cordero-Rivera, A. (2005). Evolution and ecology of Calopterygidae (Zygoptera: Odonata): Status of knowledge and research perspectives. Neotropical Entomology, 34, 861–879.CrossRefGoogle Scholar
  19. Debat, V., Bégin, M., Legout, H., & David, J. R. (2003). Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature. Evolution, 57, 2773–2784.PubMedGoogle Scholar
  20. Derryberry, E. P., Seddon, N., Claramunt, S., Tobias, J. A., Baker, A., Aleixo, A., et al. (2012). Correlated evolution of beak morphology and song in the neotropical woodcreeper radiation. Evolution, 66, 2784–2797.PubMedCrossRefGoogle Scholar
  21. DeVries, P. J., Penz, C. M., & Hill, R. I. (2010). Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies. Journal of Animal Ecology, 79, 1077–1085.PubMedCrossRefGoogle Scholar
  22. Dockx, C. (2007). Directional and stabilizing selection on wing size and shape in migrant and resident monarch butterflies, Danaus plexippus (L.), in Cuba. Biological Journal of the Linnean Society, 92, 605–616.CrossRefGoogle Scholar
  23. 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 Series B, 275, 71–76.CrossRefGoogle Scholar
  24. Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.PubMedCrossRefGoogle Scholar
  25. Dumont, H. J., Vanfleteren, J. R., De Jonckheere, J. F., & Weekers, P. H. H. (2005). Phylogenetic relationships, divergence time estimation, and global biogeographic patterns of Calopterygoid damselflies (Odonata, Zygoptera) inferred from ribosomal DNA sequences. Systematic Biology, 54, 347–362.PubMedCrossRefGoogle Scholar
  26. Dumont, H. J., Vierstraete, A., & Vanfleteren, J. R. (2010). A molecular phylogeny of the Odonata (Insecta). Systematic Entomology, 35, 6–18.CrossRefGoogle Scholar
  27. Ellington, C. P. (1984). The aerodynamics of hovering insect flight. II. Morphological parameters. Philosophical Transactions of the Royal Society Series B, 305, 17–40.CrossRefGoogle Scholar
  28. Förschler, M. I., & Bairlein, F. (2011). Morphological shifts of the external flight apparatus across the range of a passerine (northern wheatear) with diverging migratory behaviour. PLoS ONE, 6, e18732.PubMedCrossRefGoogle Scholar
  29. Garland, T., Jr, Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42, 265–292.Google Scholar
  30. Grether, G. F. (1996a). Intrasexual competition alone favors a sexually dimorphic ornament in the rubyspot damselfly Hetaerina americana. Evolution, 50, 1949–1957.CrossRefGoogle Scholar
  31. Grether, G. F. (1996b). Sexual selection and survival selection on wing coloration and body size in the rubyspot damselfly Hetaerina americana. Evolution, 50, 1939–1948.CrossRefGoogle Scholar
  32. Guan, Z., Han, B. P., Vierstraete, A., & Dumont, H. J. (2012). Additions and refinements to the molecular phylogeny of the Calopteryginae Sl (Zygoptera: Calopterygidae). Odonatologica, 41, 17–24.Google Scholar
  33. Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). New York: Springer.CrossRefGoogle Scholar
  34. Hayashi, F., Dobata, S., & Futahashi, R. (2004). Macro- and micro-scale distribution patterns of two closely related Japanese Mnais species inferred from nuclear ribosomal DNA, ITS sequences and morphology (Zygoptera: Calopterygidae). Odonatologica, 33, 399–412.Google Scholar
  35. Hedenström, A., & Møller, A. P. (1992). Morphological adaptations to song flight in passerine birds: A comparative study. Proceedings of the Royal Society Series B, 247, 183–187.CrossRefGoogle Scholar
  36. Hooper, R. E., Tsubaki, Y., & Siva-Jothy, M. T. (1999). Expression of a costly, plastic secondary sexual trait is correlated with age and condition in a damselfly with two male morphs. Physiological Entomology, 24, 364–369.CrossRefGoogle Scholar
  37. Johansson, F., Söderquist, M., & Bokma, F. (2009). Insect wing shape evolution: Independent effects of migratory and mate guarding flight on dragonfly wings. Biological Journal of the Linnean Society, 97, 362–372.CrossRefGoogle Scholar
  38. Klingenberg, C. P., & Gidaszewski, N. A. (2010). Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology, 59, 245–261.PubMedCrossRefGoogle Scholar
  39. Legagneux, P., Thery, M., Guillemain, M., Gomez, D., & Bretagnolle, V. (2010). Condition dependence of iridescent wing flash-marks in two species of dabbling ducks. Behavioural Processes, 83, 324–330.PubMedCrossRefGoogle Scholar
  40. Marchetti, K., Price, T., & Richman, A. (1995). Correlates of wing morphology with foraging behaviour and migration distance in the genus Phylloscopus. Journal of Avian Biology, 26, 177–181.CrossRefGoogle Scholar
  41. Monteiro, A., Brakefield, P. M., & French, V. (1997). The relationship between eyespot shape and wing shape in the butterfly Bicyclus anynana: A genetic and morphometrical approach. Journal of Evolutionary Biology, 10, 787–802.CrossRefGoogle Scholar
  42. Oliver, J. C., Robertson, K. A., & Monteiro, A. (2009). Accommodating natural and sexual selection in butterfly wing pattern evolution. Proceedings of the Royal Society Series B, 276, 2369–2375.CrossRefGoogle Scholar
  43. Outomuro, D., Bokma, F., & Johansson, F. (2012). Hind wing shape evolves faster than front wing shape in Calopteryx damselflies. Evolutionary Biology, 39, 116–125.CrossRefGoogle Scholar
  44. Outomuro, D., & Johansson, F. (2011). The effects of latitude, body size, and sexual selection on wing shape in a damselfly. Biological Journal of the Linnean Society, 102, 263–274.CrossRefGoogle Scholar
  45. Pajunen, V. I. (1966). Aggressive behaviour and territoriality in a population of Calopteryx virgo L. (Odon., Calopterygidae). Annales Zoologici Fennici, 3, 201–214.Google Scholar
  46. R Development Core Team. (2011). R: A language and environment for statistical computing. Version 2.15.0. Vienna: R Foundation for Statistical Computing.Google Scholar
  47. Rantala, M. J., Honkavaara, J., Dunn, D. W., & Suhonen, J. (2011). Predation selects for increased immune function in male damselflies, Calopteryx splendens. Proceedings of the Royal Society Series B, 278, 1231–1238.CrossRefGoogle Scholar
  48. Rantala, M. J., Koskimäki, J., Taskinen, J., Tynkkynen, K., & Suhonen, J. (2000). Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proceedings of the Royal Society Series B, 267, 2453–2457.CrossRefGoogle Scholar
  49. Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55, 2143–2160.PubMedGoogle Scholar
  50. Rohlf, F. J. (2004). tpsSplin. Thin-plate spline version 1.20. Available at: http://life.bio.sunysb.edu/morph/.
  51. Rohlf, F. J. (2010a). tpsDig version 2.16. Available at: http://life.bio.sunysb.edu/morph/.
  52. Rohlf, F. J. (2010b). tpsRelw. Relative warps version 1.49. Available at: http://life.bio.sunysb.edu/morph/.
  53. Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology & Evolution, 8, 129–132.CrossRefGoogle Scholar
  54. Rohlf, F. J., & Slice, D. (1990). Extension of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.CrossRefGoogle Scholar
  55. Rutowski, R. L., Nahm, A. C., & Macedonia, J. M. (2010). Iridescent hindwing patches in the pipevine swallowtail: Differences in dorsal and ventral surfaces relate to signal function and context. Functional Ecology, 24, 767–775.CrossRefGoogle Scholar
  56. Sadeghi, S., Adriaens, D., & Dumont, H. J. (2009). Geometric morphometric analysis of wing shape variation in ten European populations of Calopteryx splendens (Harris, 1782) (Zygoptera: Calopterygidae). Odonatologica, 38, 341–357.Google Scholar
  57. Serrano-Meneses, M. A., Córdoba-Aguilar, A., Azpilicueta-Amorín, M., González-Soriano, E., & Székely, T. (2008). Sexual selection, sexual size dimorphism and Rensch’s rule in Odonata. Journal of Evolutionary Biology, 21, 1259–1273.PubMedCrossRefGoogle Scholar
  58. Shingleton, A. W., Frankino, W. A., Flatt, T., Nijhout, H. F., & Emlen, D. J. (2007). Size and shape: The developmental regulation of static allometry in insects. BioEssays, 29, 536–548.PubMedCrossRefGoogle Scholar
  59. Siva-Jothy, M. T. (1999). Male wing pigmentation may affect reproductive success via female choice in a calopterygid damselfly (Zygoptera). Behaviour, 136, 1365–1377.CrossRefGoogle Scholar
  60. Siva-Jothy, M. T. (2000). A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proceedings of the Royal Society Series B, 267, 2523–2527.CrossRefGoogle Scholar
  61. Srygley, R. B. (1999). Locomotor mimicry in Heliconius butterflies: Contrast analyses of flight morphology and kinematics. Philosophical Transactions of the Royal Society Series B, 354, 203–214.CrossRefGoogle Scholar
  62. Svensson, E. I., & Friberg, M. (2007). Selective predation on wing morphology in sympatric damselflies. American Naturalist, 170, 101–112.PubMedCrossRefGoogle Scholar
  63. Svensson, E. I., & Gosden, T. P. (2007). Contemporary evolution of secondary sexual traits in the wild. Functional Ecology, 21, 422–433.CrossRefGoogle Scholar
  64. Svensson, E. I., Karlsson, K., Friberg, M., & Eroukhmanoff, F. (2007). Gender differences in species recognition and the evolution of asymmetric sexual isolation. Current Biology, 17, 1943–1947.PubMedCrossRefGoogle Scholar
  65. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.PubMedCrossRefGoogle Scholar
  66. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Clustal-W—Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.PubMedCrossRefGoogle Scholar
  67. Tsubaki, Y. (2003). The genetic polymorphism linked to mate-securing strategies in the male damselfly Mnais costalis Selys (Odonata: Calopterygidae). Population Ecology, 45, 263–266.CrossRefGoogle Scholar
  68. Tynkkynen, K., Rantala, M. J., & Suhonen, J. (2004). Interspecific aggression and character displacement in the damselfly Calopteryx splendens. Journal of Evolutionary Biology, 17, 759–767.PubMedCrossRefGoogle Scholar
  69. Waage, J. K. (1973). Reproductive behavior and its relation to territoriality in Calopteryx maculata (Beauvois) (Odonata: Calopterygidae). Behaviour, 47, 240–256.CrossRefGoogle Scholar
  70. Wakeling, J. M., & Ellington, C. P. (1997). Dragonfly flight. III. Lift and power requirements. Journal of Experimental Biology, 200, 583–600.PubMedGoogle Scholar
  71. Weekers, P. H. H., De Jonckheere, J. F., & Dumont, H. J. (2001). Phylogenetic relationships inferred from ribosomal ITS sequences and biogeographic patterns in representatives of the genus Calopteryx (Insecta: Odonata) of the West Mediterranean and adjacent West European zone. Molecular Phylogenetics and Evolution, 20, 89–99.PubMedCrossRefGoogle Scholar
  72. Wickman, P.-O. (1992). Sexual selection and butterfly design—A comparative study. Evolution, 46, 1525–1536.CrossRefGoogle Scholar
  73. Worthington, A. M., Berns, C. M., & Swallow, J. G. (2012). Size matters, but so does shape: Quantifying complex shape changes in a sexually selected trait in stalk-eyed flies (Diptera: Diopsidae). Biological Journal of the Linnean Society, 106, 104–113.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • David Outomuro
    • 1
  • Dean C. Adams
    • 2
  • Frank Johansson
    • 1
  1. 1.Department of Ecology and Genetics, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  2. 2.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA

Personalised recommendations