Abstract
Insects adapt commonly to seasonally changing habitats and reproductive contexts. Individuals that mature at different times during the year can show patterns of life cycle or morphological variation, possibly associated with changes in reproductive behaviour. Concerning mating strategies of flying insects, wing morphology may be related both to the outcome of male–male contests and to the ability in acquiring females. Therefore, different mating strategies (territorial vs. non-territorial) may have different flight morphology optima that increase fitness in their context. Males of Calopteryx splendens are mainly territorial early in the season, but with the advancing season and with increasing competition, more and more males adopt a non-territorial pursuing strategy. Given that different mating tactics have different wing morphologies, here we test whether the wing shape of males shifts from a “territorial” to a “non-territorial morphology” during the season. So, early in the season males show highly sexually dimorphic wings, which allow for high manoeuvrability and larger spots, while late in the season wing shapes of males become less sexually dimorphic and more suitable when pursuing females. Additionally, we studied the seasonal variation of other flight related traits, specifically wing lengths, abdomen length and weight. We found that these latter traits decreased along the season in both sexes without altering sexual dimorphism. However, wing shape, which resulted sexually dimorphic, showed a seasonal variation, decreasing the level of sexual dimorphism. The most probable determinant of this change is phenotypic plasticity triggered by environmental cues, but other explications of the observed pattern are discussed.
Similar content being viewed by others
References
Adams DC, Otárola-Castillo E (2013) geomorph: an r package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4:393–399. doi:10.1111/2041-210X.12035
Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the “revolution”. Ital J Zool 71:5–16. doi:10.1080/11250000409356545
Andersson M (1982) Sexual selection, natural selection and quality advertisement. Biol J Linn Soc 17:375–393. doi:10.1111/j.1095-8312.1982.tb02028.x
Berwaerts K, Van Dyck H, Aerts P (2002) Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct Ecol 16:484–491. doi:10.1046/j.1365-2435.2002.00650.x
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. Biol J Linn Soc 89:675–687. doi:10.1111/j.1095-8312.2006.00699.x
Betts CR, Wootton RJ (1988) Wing shape and flight behaviour in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): a preliminary analysis. J Exp Biol 138:271–288
Bookstein FL (1997) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge
Bots J, Breuker CJ, Van Kerkhove A et al (2009) Variation in flight morphology in a female polymorphic damselfly: intraspecific, intrasexual, and seasonal differences. Can J Zool 87:86–94. doi:10.1139/Z08-141
Brakefield PM, Larsen TB (1984) The evolutionary significance of dry and wet season forms in some tropical butterflies. Biol J Linn Soc 22:1–12. doi:10.1111/j.1095-8312.1984.tb00795.x
Brockmann HJ (2001) The evolution of alternative strategies and tactics. Adv Stud Behav 30:1–51. doi:10.1016/S0065-3454(01)80004-8
Chown SL, Gaston KJ (2010) Body size variation in insects: a macroecological perspective. Biol Rev Camb Philos Soc 85:139–169. doi:10.1111/j.1469-185X.2009.00097.x
Cigognini R, Gallesi MM, Mobili S et al (2014) Does character displacement demonstrate density-dependent expression in females? A test on the wing shape of two species of European damselflies. Evol Ecol 28:941–956. doi:10.1007/s10682-014-9711-1
Claude J (2008) Morphometrics with R. Springer, New York
Corbet PS (1999) Dragonflies: behavior and ecology of Odonata. Cornell University Press, New York
Cordero-Rivera A (1999) Forced copulations and female contact guarding at a high male density in a calopterygid damselfly. J Insect Behav 12:27–37. doi:10.1023/A:1020972913683
Cordero-Rivera AR, Andrés JA (2002) Male coercion and convenience polyandry in a calopterygid damselfly. J Insect Sci 2:14. doi:10.1093/jis/2.1.14
Córdoba-Aguilar A, Cordero-Rivera A (2005) Evolution and ecology of Calopterygidae (Zygoptera: Odonata): status of knowledge and research perspectives. Neotrop Entomol 34:861–879. doi:10.1590/S1519-566X2005000600001
Cotton S, Fowler K, Pomiankowski AP (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271:771–783. doi:10.1098/rspb.2004.2688
Dijkstra K-DB, Lewington R (2006) Field guide to the dragonflies of Britain and Europe: including Western Turkey and North-western Africa. British Wildlife Publishing, Dorset
Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, Chichester
Dudley R (2002) The biomechanics of insect flight: form, function, evolution. Princeton University Press, Princeton
Dumont HJ (1991) Odonata of the Levant. Israel academy of sciences and humanities, Jerusalem, IL
Forsyth A, Montgomerie RD (1987) Alternative reproductive tactics in the territorial damselfly Calopteryx maculata: sneaking by older males. Behav Ecol Sociobiol 21:73–81. doi:10.1007/PL00020230
Gotthard K, Nylin S (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3–17. doi:10.2307/3545669
Gotthard K, Nylin S, Wiklund C (1994) Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99:281–289. doi:10.1007/BF00627740
Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546. doi:10.1016/S0022-5193(05)80088-8
Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11(2):92–98. doi:10.1016/0169-5347(96)81050-0
Hardersen S (2010) Seasonal variation of wing spot allometry in Calopteryx splendens (Odonata Calopterygidae). Ethol Ecol Evol 22:365–373. doi:10.1080/03949370.2010.510042
Hardersen S, Wratten SD, Frampton CM (1999) Does carbaryl increase fluctuating asymmetry in damselflies under field conditions? A mesocosm experiment with Xanthocnemis zealandica (Odonata: Zygoptera). J Appl Ecol 36:534–543. doi:10.1046/j.1365-2664.1999.00417.x
Hilfert D, Rüppell G (1997) Alternative mating tactics in Calopteryx splendens (Odonata: Calopterygidae). Mitt Dtsch Ges Allg Angew Ent 11:411–414
Hilfert-Rüppell D, Rüppell G (2009) Males do not catch up with females in pursuing flight in Calopteryx splendens (Odonata: Calopterygidae). Int J Odonatol 12:195–203. doi:10.1080/13887890.2009.9748339
Johansson F, Söderquist M, Bokma F (2009) Insect wing shape evolution: independent effects of migratory and mate guarding flight on dragonfly wings. Biol J Linn Soc 97:362–372. doi:10.1111/j.1095-8312.2009.01211.x
Kemp DJ, Alcock J (2003) Lifetime resource utilization, flight physiology, and the evolution of contest competition in territorial insects. Am Nat 162:290–301. doi:10.1086/376890
Kemp DJ, Wiklund C (2004) Residency effects in animal contests. Proc R Soc Lond B 271:1707–1712. doi:10.1098/rspb.2004.2775
Kingsolver JG (1995) Viability selection on seasonally polyphenic traits: wing melanin pattern in western white butterflies. Evolution 49:932–941. doi:10.2307/2410415
Kingsolver JG, Wiernasz DC (1991) Seasonal polyphenism in wing-melanin pattern and thermoregulatory adaptation in Pieris butterflies. Am Nat 137:816–830
Koskimäki J, Rantala MJ, Taskinen J et al (2004) Immunocompetence and resource holding potential in the damselfly, Calopteryx virgo L. Behav Ecol 15:169–173. doi:10.1093/beheco/arg088
Marden JH, Waage JK (1990) Escalated damselfly territorial contests are energetic wars of attrition. Anim Behav 39:954–959. doi:10.1016/S0003-3472(05)80960-1
Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18. doi:10.1046/j.1525-142X.2003.03003.x
Nylin S (1994) Seasonal plasticity and life-cycle adaptations in butterflies. In: Danks HV (ed) Insect life-cycle polymorphism. Springer Netherlands, Dordrecht, pp 41–67
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83. doi:10.1146/annurev.ento.43.1.63
Oliveira RF, Taborsky M, Brockmann HJ (2008) Alternative reproductive tactics: an integrative approach. Cambridge University Press, New York
Outomuro D, Johansson F (2011) The effects of latitude, body size, and sexual selection on wing shape in a damselfly. Biol J Linn Soc 102:263–274. doi:10.1111/j.1095-8312.2010.01591.x
Outomuro D, Bokma F, Johansson F (2012) Hind wing shape evolves faster than front wing shape in Calopteryx damselflies. Evol Biol 39:116–125. doi:10.1007/s11692-011-9145-4
Outomuro D, Adams DC, Johansson F (2013a) The evolution of wing shape in ornamented-winged damselflies (Calopterygidae, Odonata). Evol Biol 40:1–10. doi:10.1007/s11692-012-9214-3
Outomuro D, Adams DC, Johansson F (2013b) Wing shape allometry and aerodynamics in calopterygid damselflies: a comparative approach. BMC Evol Biol 13:118. doi:10.1186/1471-2148-13-118
Outomuro D, Rodríguez-Martínez S, Karlsson A, Johansson F (2014) Male wing shape differs between condition-dependent alternative reproductive tactics in territorial damselflies. Anim Behav 91:1–7. doi:10.1016/j.anbehav.2014.02.018
Plaistow S, Siva-Jothy MT (1996) Energetic constraints and male mate-securing tactics in the damselfly Calopteryx splendens xanthostoma (Charpentier). Proc R Soc Lond B Biol 263:1233–1239. doi:10.1098/rspb.1996.0181
Plaistow SJ, Johnstone RA, Colegrave N, Spencer M (2004) Evolution of alternative mating tactics: conditional versus mixed strategies. Behav Ecol 15(4):534–542. doi:10.1093/beheco/arh029
Rantala MJ, Honkavaara J, Suhonen J (2010) Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx splendens by birds. Oecologia 163:825–832. doi:10.1007/s00442-010-1582-8
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rohlf JF (2010) tpsDig2. Department of Ecology and Evolution, State University of New York, Stony Brook
Rohlf JF, Marcus LF (1993) A revolution morphometrics. Trends Ecol Evol 8:129–132. doi:10.1016/0169-5347(93)90024-J
Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Biol 39:40–59. doi:10.2307/2992207
Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427. doi:10.2307/2937184
Sacchi R, Hardersen S (2013) Wing length allometry in Odonata: differences between families in relation to migratory behaviour. Zoomorphology 132:23–32. doi:10.1007/s00435-012-0172-1
Shapiro AM (1976) Seasonal polyphenism. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology. Springer, US, pp 259–333
Siva-Jothy MT (2000) A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proc R Soc Lond B Biol 267:2523–2527. doi:10.1098/rspb.2000.1315
Stoks R, Johansson F, De Block M (2008) Life-history plasticity under time stress in damselfly larvae. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies: model organisms for ecological and evolutionary research. Oxford University Press, Oxford, pp 39–50
Sweeney BW, Vannote RL (1978) Size variation and the distribution of hemimetabolous aquatic insects: two thermal equilibrium hypotheses. Science 200:444–446. doi:10.1126/science.200.4340.444
Van Dyck H, Wiklund C (2002) Seasonal butterfly design: morphological plasticity among three developmental pathways relative to sex, flight and thermoregulation. J Evol Biol 15:216–225. doi:10.1046/j.1420-9101.2002.00384.x
Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214. doi:10.1016/0022-5193(75)90111-3
Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgments
We would like to thank Elisa Riservato for her support and for the suggestions about the sampling site, and for her help and advice during the sampling. Also, thanks go to Fabio Pupin for the help during the field work. We want to thank also two anonymous reviewers that helped us to improve the manuscript.
Funding
This study was partially supported by a PhD grant of the University of Pavia to M.M.G.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Additional information
Communicated by A. Schmidt-Rhaesa.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gallesi, M.M., Mobili, S., Cigognini, R. et al. Season matters: differential variation of wing shape between sexes of Calopteryx splendens (Odonata: Calopterygidae). Zoomorphology 135, 313–322 (2016). https://doi.org/10.1007/s00435-016-0309-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-016-0309-8