Skip to main content
SpringerLink
Log in

Patterns of Phenotypic Divergence in Wing Covariance Structure of Calopterygid Damselflies

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Comparing species differences in covariance patterns of traits subject to divergent selection pressures can increase our understanding to the mechanisms of phenotypic divergence. Different species of calopterygid damselflies have diverged in the melanized wing patch of males. This trait serves multiple ecological functions and has behavioral consequences in terms of sexual selection, interspecific interactions, reproductive isolation. We compared the phenotypic variance-covariance matrices (P) of wing traits among nine populations of four European species of calopterygid damselflies. We found modest divergence in covariance structure among populations of the same species, but strong divergence between species. Interestingly, the orientation of the first eigenvector of P (P max ) differed more between closely related species than between distantly related species, although this pattern was absent when overall covariance structures were compared. We also found that distantly related species but geographically closer had converged towards a similar covariance structure. Finally, divergence in covariance structure was correlated with divergence in wing patch length, but not with other wing traits. This last finding suggests that divergent selection on wing patch length might have affected the stability of P. These results indicate that P might not only reflect ancestral developmental pathways but might also be influenced by current ecology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arnold, S. J. (1992). Constraints on phenotypic evolution. American Naturalist, 140, S85–S107. doi:10.1086/285398.

    Article  Google Scholar 

  • Arnold, S. J., Burger, R., Holenhole, P. A., Beverley, C. A., & Jones, A. G. (2008). Understanding the evolution and stability of the G-matrix. Evolution; International Journal of Organic Evolution, 62, 2451–2461. doi:10.1111/j.1558-5646.2008.00472.x.

    PubMed  Google Scholar 

  • Arnold, S. J., Pfrender, M. E., & Jones, A. G. (2001). The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica, 112–113, 9–32. doi:10.1023/A:1013373907708.

    Article  PubMed  Google Scholar 

  • Askew, R. R. (1988). The dragonflies of Europe. Colchester, UK: Harley books.

    Google Scholar 

  • Beldade, P., Koops, K., & Brakefield, P. M. (2002). Developmental constraints versus flexibility in morphological evolution. Nature, 416, 844–847. doi:10.1038/416844a.

    Article  PubMed  CAS  Google Scholar 

  • Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155–172. doi:10.1016/S0022-5193(84)80050-8.

    Article  PubMed  CAS  Google Scholar 

  • Cheverud, J. M. (1996). Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. Journal of Evolutionary Biology, 9, 5–42. doi:10.1046/j.1420-9101.1996.9010005.x.

    Article  Google Scholar 

  • Clusella-Trullas, S., van Wyk, J. H., & Spotila, J. R. (2007). Thermal melanism in ectotherms. Journal of Thermal Biology, 32, 235–245. doi:10.1016/j.jtherbio.2007.01.013.

    Article  Google Scholar 

  • Corbet, P. S. (1999). Dragonflies: Behaviour and ecology of Odonata. Colchester, UK: Harley Books.

    Google Scholar 

  • 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. doi:10.1590/S1519-566X2005000600001.

    Article  Google Scholar 

  • Debat, V., Begin, M., Legout, H., & David, J. R. (2003). Allometric and nonallometric components of Drosophila wing shape respond differently to developmental temperature. Evolution; International Journal of Organic Evolution, 57, 2773–2784.

    PubMed  Google Scholar 

  • Debat, V., & David, P. (2001). Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution, 16, 555–561. doi:10.1016/S0169-5347(01)02266-2.

    Article  Google Scholar 

  • Debat, V., Milton, C. C., Rutherford, S., Klingenberg, C. P., & Hoffmann, A. A. (2006). Hsp90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution; International Journal of Organic Evolution, 60, 2529–2538.

    PubMed  CAS  Google Scholar 

  • Dumont, H. J., Mertens, J., & De Coster, W. (1993). The Calopteryx-splendens-cline in southwestern France, analysed by quantitative wingspot analysis (Zygoptera: Calopterygidae). Odonatologica, 22, 345–351.

    Google Scholar 

  • 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. doi:10.1080/10635150590949869.

    Article  PubMed  Google Scholar 

  • Eroukhmanoff, F., & Svensson, E. I. (2008). Phenotypic integration and conserved covariance structure in calopterygid damselflies. Journal of Evolutionary Biology, 21, 514–526. doi:10.1111/j.1420-9101.2007.01488.x.

    Article  PubMed  CAS  Google Scholar 

  • Frankino, W. A., Zwaan, B. J., Stern, D. L., & Brakefield, P. M. (2005). Natural selection and developmental constraints in the evolution of allometries. Science, 307, 718–720. doi:10.1126/science.1105409.

    Article  PubMed  CAS  Google Scholar 

  • Funk, D. J., Nosil, P., & Etges, W. J. (2006). Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proceedings of the National Academy of Sciences of the United States of America, 103, 3209–3213. doi:10.1073/pnas.0508653103.

    Article  PubMed  CAS  Google Scholar 

  • Game, E. T., & Caley, M. J. (2006). The stability of P in coral reef fishes. Evolution; International Journal of Organic Evolution, 60, 814–823.

    PubMed  Google Scholar 

  • Goodin, J. T., & Johnson, M. S. (1992). Patterns of morphological covariation in Partula. Systematic Biology, 41, 292–304. doi:10.2307/2992568.

    Google Scholar 

  • Hedenstrom, A., & Rosen, M. (2001). Predator versus prey: On aerial hunting and escape strategies in birds. Behavioral Ecology, 12, 150–156. doi:10.1093/beheco/12.2.150.

    Article  Google Scholar 

  • Huey, R. B., Gilchrist, G. W., Carlson, M. L., Berrigan, D., & Serra, L. (2000). Rapid evolution of a geographic cline in size in an introduced fly. Science, 287, 308–309. doi:10.1126/science.287.5451.308.

    Article  PubMed  CAS  Google Scholar 

  • Jamniczky, H. A., & Hallgrimsson, B. (2009). A comparison of covariance structure of wild and laboratory muroid crania. Evolution: International Journal of Organic Evolution. doi:10.1111/j.1558-5646.2009.00651.x.

    Google Scholar 

  • Marden, J. H. (2008). Dragonfly flight performance: a model system for biomechanics, physiological genetics, and animal competitive behaviour, Chap. 19, pp. 249–259. In A. Córdoba-Aguilar (Ed.), Dragonflies and damselflies: Model organisms for ecological and evolutionary research. Oxford: Oxford University Press.

    Google Scholar 

  • Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., et al. (1985). Developmental constraints and evolution: A perspective from the mountain lake conference on development and evolution. Quarterly Review of Biology, 60, 265–287.

    Article  Google Scholar 

  • McGhee, G. R. (1999). Theoretical morphology: The concept and its applications. New York: Columbia University Press.

    Google Scholar 

  • Nijhout, H. F. (2008). Developmental phenotypic landscapes. Evolutionary Biology, 35, 100–103. doi:10.1007/s11692-008-9024-9.

    Article  Google Scholar 

  • Pelabon, C., Hansen, T. F., Carter, A. J., & Houle, D. (2006). Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster. Journal of Evolutionary Biology, 19, 764–776. doi:10.1111/j.1420-9101.2005.01054.x.

    Article  PubMed  CAS  Google Scholar 

  • Polly, P. D. (2008). Developmental dynamics and G-matrices: Can morphometric spaces be used to model phenotypic evolution? Evolutionary Biology, 35, 83–96. doi:10.1007/s11692-008-9020-0.

    Article  Google Scholar 

  • Revell, L. J. (2007). Skewers. Available via http://anolis.oeb.harvard.edu/~liam/programs/.

  • Riska, B. (1985). Group size factors and geographic variation of morphometric correlation. Evolution; International Journal of Organic Evolution, 39, 792–803. doi:10.2307/2408679.

    Google Scholar 

  • Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution; International Journal of Organic Evolution, 50, 1766–1774. doi:10.2307/2410734.

    Google Scholar 

  • Schluter, D. (2000). The ecology of adaptive radiation. New York: Oxford University Press Inc.

    Google Scholar 

  • Simon, J. L. (2000). Resampling Stats 2000. Virginia: Resampling Stats.

    Google Scholar 

  • Sinervo, B., & Svensson, E. (2002). Correlational selection and the evolution of genomic architecture. Heredity, 89, 329–338. doi:10.1038/sj.hdy.6800148.

    Article  PubMed  CAS  Google Scholar 

  • Siva-Jothy, M. T. (1999). Male wing pigmentation may affect reproductive success via female choice in a calopterygid damselfly (Zygoptera). Behaviour, 136, 1365–1377. doi:10.1163/156853999500776.

    Article  Google Scholar 

  • Statsoft, Inc. STATISTICA [7]. (2004). Statsoft, I. Available at: www.statsoft.com.

  • Steppan, S. J. (1997). Phylogenetic analysis of phenotypic covariance structure. 2. Reconstructing matrix evolution. Evolution; International Journal of Organic Evolution, 51, 587–594. doi:10.2307/2411130.

    Google Scholar 

  • Svensson, E. I., Eroukhmanoff, F., & Friberg, M. (2006). Effects of natural and sexual selection on adaptive population divergence and premating isolation in a damselfly. Evolution; International Journal of Organic Evolution, 60, 1242–1253.

    PubMed  Google Scholar 

  • Svensson, E. I., & Friberg, M. (2007). Selective predation on wing morphology in sympatric damselflies. American Naturalist, 170, 101–112.

    Article  PubMed  Google Scholar 

  • 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. doi:10.1016/j.cub.2007.09.038.

    Article  PubMed  CAS  Google Scholar 

  • Svensson, E. I., Kristoffersen, L., Oskarsson, K., & Bensch, S. (2004). Molecular population divergence and sexual selection on morphology in the banded demoiselle (Calopteryx splendens). Heredity, 93, 423–433. doi:10.1038/sj.hdy.6800519.

    Article  PubMed  CAS  Google Scholar 

  • True, J. R., Edwards, K. A., Yamamoto, D., & Carroll, S. B. (1999). Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Current Biology, 9, 1382–1391. doi:10.1016/S0960-9822(00)80083-4.

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1111/j.1420-9101.2004.00733.x.

    Article  PubMed  CAS  Google Scholar 

  • Usherwood, J. R., & Lehmann, F. (2008). Phasing of dragonfly wings can improve aerodynamic efficiency by removing swirl. Journal of the Royal Society, Interface, 5, 1303–1307. doi:10.1098/rsif.2008.0124.

    Article  PubMed  Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Perspective: Complex adaptations and the evolution of evolvability. Evolution; International Journal of Organic Evolution, 50, 967–976. doi:10.2307/2410639.

    Google Scholar 

  • Wagner, G. P., Booth, G., & Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution; International Journal of Organic Evolution, 51, 329–347. doi:10.2307/2411105.

    Google Scholar 

  • Wallace, A. (2009). The effect of development on the direction of evolution: Toward a twenty-first century consensus. Evolution & Development, 6, 282–288.

    Google Scholar 

  • 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. doi:10.1006/mpev.2001.0947.

    Article  PubMed  CAS  Google Scholar 

  • West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York: Oxford University Press Inc.

    Google Scholar 

  • Willmore, K. E., Young, N. M., & Richtsmeier, J. T. (2007). Phenotypic variability: Its Components, measurement and underlying developmental processes. Evolutionary Biology, 34, 99–120. doi:10.1007/s11692-007-9008-1.

    Article  Google Scholar 

  • Wotton, R. J., & Newman, D. J. S. (2008). Evolution, diversification, and mechanics of dragonfly wings, Chap. 20, pp. 261–274. In A. Córdoba-Aguilar (Ed.), Dragonflies and damselflies Model organisms for ecological and evolutionary research. Oxford: Oxford University Press.

    Google Scholar 

  • Zera, A. J. (2006). Evolution genetics of juvenile hormone and ecdysteroid regulation in Gryllus: A case study in the microevolution of endocrine regulation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 144, 365–379. doi:10.1016/j.cbpa.2005.11.026.

    Article  Google Scholar 

  • Zera, A. J., Potts, J., & Kobus, K. (1998). The physiology of life-history trade-offs: Experimental analysis of a hormonally induced life-history trade-off in Gryllus assimilis. American Naturalist, 152, 7–23. doi:10.1086/286146.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to S. Kuchta, T. Gosden and two anonymous referees for constructive criticisms on the early drafts of this manuscript. This study was financially supported by The Ecole Normale Supérieure (ENS) and The Royal Physiographic Society in Lund (KFS) to FE, by the Fundación para el Fomento en Asturias de la Invetigación Cientifica Aplicada y la Tecnología (FICYT) to DO and the Swedish Research Council (VR) and The Swedish Council for Environment, Agriculture, and Spatial Planning (FORMAS) to EIS.

Author information

Authors and Affiliations

  1. Section for Animal Ecology, Ecology Building, Lund University, 223 62, Lund, Sweden

    Fabrice Eroukhmanoff & Erik I. Svensson

  2. Departamento de Biología de Organismos y Sistemas, Oviedo University, 33071, Oviedo, Spain

    David Outomuro & Francisco J. Ocharan

Authors
  1. Fabrice Eroukhmanoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Outomuro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francisco J. Ocharan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erik I. Svensson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabrice Eroukhmanoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eroukhmanoff, F., Outomuro, D., Ocharan, F.J. et al. Patterns of Phenotypic Divergence in Wing Covariance Structure of Calopterygid Damselflies. Evol Biol 36, 214–224 (2009). https://doi.org/10.1007/s11692-009-9057-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-009-9057-8

Keywords

Search

Navigation